Key Laboratory of Subsurface Hydrology and Ecological Effect in Arid Region, Ministry of Education, School of Water and Environment, Chang’an University, Xi’an 710054, China
2.
School of Biological and Environmental Engineering, Xi’an University, Xi’an 710065, China
3.
Environmental Monitoring Station of Lanshan Branch, Rizhao Bureau of Ecology and Environment, Rizhao 276800, China
4.
Yunnan Key Laboratory of Earth System Science, Yunnan University, Kunming 650500, China
Zhoufeng Wang is a lecturer with Chang’an University. He received his Ph.D. degree from the Institute of Earth Environment, Chinese Academy of Sciences, in July 2008, and joined Chang’an University in the same year. His research interests focus on stable nitrogen isotope in the plant-soil system and the coupling mechanism of water, air, and heat transport in the critical zone
Petroleum contamination in terrestrial environments caused by industrial activities is a significant problem that has received considerable attention. Carbon and nitrogen isotopic compositions (δ13C and δ15N) effectively describe the behavior of plants and soils under petroleum contamination stress. To better understand plant and soil responses to petroleum-contaminated soil, δ13C and δ15N values of the plants (Trifolium repens, Leguminosae with C3 photosynthesis pathway, and Agropyron cristatum with C4 photosynthesis pathway) and the soil samples under one-month exposure to different extents of petroleum contamination were measured. The results showed that petroleum contamination in the soil induced the soil δ15N values to increase and δ13C values to decrease; from 1.9‰ to 3.2‰ and from −23.6‰ to −26.8‰, respectively. However, the δ13C values of Agropyron cristatum decreased from −29.8‰ to −31.6‰, and the δ13C values of Trifolium repens remained relatively stable from −12.6‰ to −13.1‰, indicating that they have different coping strategies under petroleum-contaminated soil conditions. Moreover, the δ15N values of Trifolium repens decreased from 5.6‰ to 0.8‰ near the air δ15N values under petroleum-contaminated soil, which implies that their nitrogen fixation system works to reduce soil petroleum stress. The δ13C and δ15N values of Agropyron cristatum and Trifolium repens reflect changes in the metabolic system when they confront stressful environments. Therefore, stable isotopic compositions are useful proxies for monitoring petroleum-contaminated soil and evaluating the response of plants to petroleum contamination stress.
Graphical Abstract
The δ13C and δ13N values of soil and plant changed with petroleum-contaminated soil concentration.
Abstract
Petroleum contamination in terrestrial environments caused by industrial activities is a significant problem that has received considerable attention. Carbon and nitrogen isotopic compositions (δ13C and δ15N) effectively describe the behavior of plants and soils under petroleum contamination stress. To better understand plant and soil responses to petroleum-contaminated soil, δ13C and δ15N values of the plants (Trifolium repens, Leguminosae with C3 photosynthesis pathway, and Agropyron cristatum with C4 photosynthesis pathway) and the soil samples under one-month exposure to different extents of petroleum contamination were measured. The results showed that petroleum contamination in the soil induced the soil δ15N values to increase and δ13C values to decrease; from 1.9‰ to 3.2‰ and from −23.6‰ to −26.8‰, respectively. However, the δ13C values of Agropyron cristatum decreased from −29.8‰ to −31.6‰, and the δ13C values of Trifolium repens remained relatively stable from −12.6‰ to −13.1‰, indicating that they have different coping strategies under petroleum-contaminated soil conditions. Moreover, the δ15N values of Trifolium repens decreased from 5.6‰ to 0.8‰ near the air δ15N values under petroleum-contaminated soil, which implies that their nitrogen fixation system works to reduce soil petroleum stress. The δ13C and δ15N values of Agropyron cristatum and Trifolium repens reflect changes in the metabolic system when they confront stressful environments. Therefore, stable isotopic compositions are useful proxies for monitoring petroleum-contaminated soil and evaluating the response of plants to petroleum contamination stress.
Public Summary
Petroleum-contaminated soil induced the soil δ15N values to increase and δ13C values to decrease.
The characteristics of plants influence plant δ13C and δ15N values under petroleum-contaminated soil.
The δ13C and δ15N values are useful proxies for monitoring petroleum-contaminated soil and evaluating the response of plants to the stress of petroleum contamination.
Contamination of soils and groundwater aquifers is a major problem in locations near industrial and urban areas[1−4]. An increasing number of sites are seriously contaminated by petroleum hydrocarbon pollutants due to industrial activities such as vehicle transit paths, pipes for petroleum transport, boat shoring sites, and oil tank replenishment and storage areas, as confirmed by academic and government organizations in the USA, Western Europe, Nigeria, China, etc.[5−8]. As a complex mixture of compounds, petroleum includes both branched and straight-chain alkanes and polycyclic aromatic hydrocarbons (PAHs)[9]. Petroleum compounds are carcinogenic, mutagenic, and teratogenic and are classified as priority environmental pollutants due to their persistence and recalcitrance[10−12]. In addition, petroleum compounds that enter soil and water adversely affect soil safety, plant growth and development, and human health [13, 14]. Therefore, accurately tracking complex petroleum pollutants in soil and plant systems is important for petroleum contamination assessment[14−16].
A series of biologically mediated chemical reactions occur when petroleum enters the soil, during which petroleum compounds can be converted into intermediate metabolites and subsequent end products via various enzymatic pathways without any long-term adverse effects on affected environments[17, 18]. For example, Nocardia soli Y48, a strain of Actinobacteria isolated from the Qinghai-Tibetan Plateau, can degrade nearly all components of crude oil through hydrocarbon degradation, biosurfactant synthesis, emulsification, and other related metabolic pathways [19]. Pereira et al.[20] found that Bacillus methylotrophicus and Pseudomonas sihuiensis can degrade medium (C8–C19) and long (C20–C33) chain aliphatic hydrocarbons, isoprenoids, anthracene, phenanthrene, and pyrene by producing biosurfactants that can reduce the surface tension and pH of aliphatic compounds and PAHs. Moreover, rhizoremediation is an attractive strategy that enhances microbial populations and activities of PAH-contaminated soils through plant root exudates[21]. The types of microorganisms[22, 23], soil physical and chemical features (such as pH, water content, oxygen availability, nutrient availability, salinity, etc.) [24, 25], and the surrounding environment affect the environmental behavior of petroleum compounds in soil[26−29], thus, further impacting plants, which depend on good soil quality for survival. However, an accurate description of petroleum environmental behavior and its impact in extreme environments (i.e., water scarcity, drought, and cold conditions) requires additional studies. A more useful monitoring index is required to monitor the response of plants and soil to petroleum contamination.
The stable or radioactive isotope-labeled techniques are useful in tracking sources and fates of organic compounds in the environment[30−32]. Substantial isotopic fractionation during the microbial degradation of the investigated compounds can help identify, qualify, and assess biodegradation[33−35]. Environmental conditions affect the fractionation of C isotopes of PAHs during the formation, transportation, and degradation processes[36]. Under anaerobic conditions, the δ13C values of methyl tert-butyl ether (MTBE) increased from −31.4‰ to −11.8‰, indicating MTBE degradation[37]. Generally, lighter isotopes exhibit faster reaction rates than heavier isotopologues during the biodegradation of organic compounds[38, 39]. Phase transfer (e.g., sorption, volatilization), transport processes (diffusion), chemical bond cleavage, or formation all result in isotopic fractionation [40]. Notably, δ2H and δ13C have been used to source the apportionment of polycyclic aromatic hydrocarbons[41, 42]. Nitrogen (N) is one of the essential nutrients for soil microorganisms and plants. However, soil pollution by organic or inorganic components affects the quantity and activity of soil microorganisms, which can influence nitrogen mineralization and nitrogen uptake by plants. As one of the important trace marks for nitrogen cycling, stable isotopic compositions of nitrogen have been used to trace nitrogen transfer in soil-plant systems. However, there have not been enough studies to assess δ15N changes under petroleum contamination conditions in soil and plants. Therefore, it is of interest to know whether δ13C and δ15N have potential as useful indices for plants and soil under petroleum-contaminated soil, which may provide some clues for soil and plants in polluted conditions.
In arid and semiarid areas, water scarcity and poor soil quality are unfavorable for microorganisms to degrade petroleum contaminants in the soil. In the Ordos Basin, an important energy and chemical industry base abundant in coal, gas, and oil in China, environmentally friendly and cost-efficient bioremediation techniques are needed for this fragile ecosystem[43, 44]. Two kinds of plants, Agropyron cristatum with the C4 photosynthesis pathway and Trifolium repens with the C3 photosynthesis pathway and nitrogen fixation ability, which adapt to arid and semi-arid environments, were used to compare plant responses to petroleum-contaminated soil. The major aims of this study were ① to identify whether δ13C and δ15N in soils and plants can be used as a specific index to trace petroleum-contaminated soil and ② to compare the different responses of plants to different soil petroleum concentrations.
2.
Materials and methods
2.1
Study site
The field experiment was conducted at the Demonstration Field of Water and Environment (34°16′ N, 108°56′ E) at Chang’an University, Xi’an, China. The experimental site is located in the middle of the Guanzhong Basin, with an elevation of 400 m and a temperate continental climate. The annual mean temperature and precipitation are 13 °C and 600 mm, respectively [45].
2.2
Experimental design and sample collection
Silty loam soil used in this study was collected from the Loess Plateau of Gaoling, north of Xi’an City, Shaanxi Province, China. The chemical and physical properties of the soil were measured[46] (Table 1). According to the World Reference Base for Soil Resources (WRB), soil can be classified as Calciustepts and Haplic Calcisols[47].
Table
1.
General physical and chemical properties of experimental soil.
Before the experiment, the soil was sieved with a 2 mm sieve to remove big rocks and other debris. Then the soil was put into 12 experiment quadrats made of brick and cement with 1 m length ×1 m width × 0.9 m height. To monitor the effects of petroleum contamination on soil and plants, crude oil taken from a petroleum extraction factory was added and mixed with 20 cm surface soil. The petroleum gradients were designed as 0 (control), 3000, 7000, and 10000 mg/kg (Table 2).
Table
2.
Experimental design for petroleum concentration in the soil. Twelve quadrats were used in the experiment.
Agropyron cristatum and Trifolium repens were used as experimental plants to monitor the response and changes of δ13C and δ15N of the plant under different soil petroleum concentrations. The two kinds of experimental plants were planted on August 11, 2010. After one month of plant growing and contaminating exposure, soil and plant samples were collected from 12 quadrats for further analysis (Fig. 1). About 500 g of the petroleum-contaminated soil samples were collected using a shovel and oven-dried (40 ℃) for 72 h. Then the soils were ground in an agate mill and sieved with a 0.2 mm sieve for further analysis. For Agropyron cristatum and Trifolium repens, both the leaf and root were collected from the experimental field (Fig. 1). Then the plant was cleaned using deionized water and oven-dried (40 ℃) for 72 h. Three to five whole plants were pulled together as one testing sample, and all samples were ground in an agate mill for further analysis.
Figure
1.
The Trifolium repens (a) and Agropyron cristatum (b) were collected from the experimental field after one month of growth. 0, 3000, 7000, and 10000 in the picture means the petroleum contamination concentration in the soil increased from 0, 3000, 7000 to 10000 mg/kg, respectively.
The δ15N values of the plants and soil were analyzed at the Isotope Laboratory of the Institute of Earth Environment, Chinese Academy of Sciences, Shaanxi Province, China. A CE FLASH 1112 elemental analyzer (CE Instruments, Rodano, Italy) equipped with an AS200 auto-sampler interfaced with a Delta PLUS isotope-ratio mass spectrometer via a Finnigan Conflo III interface (ThermoQuest, Finnigan, Germany) was used to determine the δ15N and nitrogen contents of the samples[48]. The δ15N values were calculated using the following equation:
δ15N(‰)=(RsampleRstandard−1)×1000,
where Rsample and Rstandard are the 15N/14N ratios of the sample and standard, respectively. The δ15N values are reported relative to the atmospheric N2 isotopic standard. During the laboratory measurements, soil produced by the laboratory with known δ15N values (δ15N = 5.46‰ ± 0.16‰) was used as an in-house standard to link the δ15N values to atmospheric N2 and monitor analytical accuracy. Long-term analysis of the in-house standard showed stability and reliability. The standard deviation for duplicate analysis was less than 0.3‰ for δ15N. The difference between the δ15N of plants and soil is denoted as ∆15Nplant-soil.
2.4
Carbon isotope ratio (δ13C) analysis
To remove the soil carbonate, approximately 3 g of soil samples were treated with 2 mol/L HCl for 24 h. Then, the samples were rinsed to pH > 4 with distilled water and dried at 60 ℃ [49].
The plant and soil samples were sealed using a quartz tube with copper oxide and silver foil under vacuum conditions. Consequently, the quartz tube was combusted for at least 4 h at 800–850 ℃. The CO2 gas from the combustion tube was extracted and purified cryogenically for isotopic analysis[50].
Carbon isotope ratios (δ13C) were analyzed at the Isotope Laboratory of the Institute of Earth Environment, Chinese Academy of Sciences, Shaanxi Province, China. A MAT-251 gas mass spectrometer equipped with a dual-inlet system analyzed the soil and plant samples[49]. The carbon isotope results are expressed in delta (δ) notation relative to the V-PDB standard, and the standard deviation for duplicate analysis was less than ±0.2‰.
2.5
Data analysis
One-way ANOVA statistical analyses and Duncan’s multiple test range tests of the experimental data were used to determine whether there was a statistically significant difference between the medians of three or more independent groups; the different letters (a, b, or c) in figures indicate significant differences among petroleum contamination concentrations in the soil. The minimum level of significance of the results was set at p < 0.05.
3.
Results
3.1
δ13C and δ15N variation in plants under different petroleum pollution concentration
Fig. 2 shows the variations in the δ13C values of soil with and without plants under different soil petroleum pollution concentrations. In petroleum-contaminated soil without plant disturbance, soil δ13C values linearly decreased as the soil petroleum concentration increased. The δ13C values of soil organic matter ranged from −23.6‰ to −26.8‰ with an average value of −25.2‰, which is lower than the δ13C values of the original soil (−21.3‰) but higher than the δ13C values of petroleum (−32‰). The soil δ13C values decreased as the soil petroleum concentration increased when Agropyron cristatum and Trifolium repens were planted. However, compared with Trifolium repens planted quadrats, the soil δ13C values in the Agropyron cristatum plantation changed significantly.
Figure
2.
Soil δ13C variations under different petroleum pollution conditions with and without plants. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations ( p < 0.05).
Fig. 3 shows the soil δ15N values with and without petroleum contamination. The soil δ15N values increased as soil petroleum concentration increased without plant conditions, and the soil δ15N values varied, ranging from 1.9‰ to 3.2‰ with an average value of 2.7‰. Under Trifolium repens plantation, the soil δ15N values were close to 3.0‰. Except for 3000 mg/kg petroleum-contaminated soil with Agropyron cristatum planted, soil δ15N values were lower than petroleum pollution with Trifolium repens planted. The δ15N values of Loess and organic fertilizer in the experiment are 2.2‰ and 3.8‰, respectively.
Figure
3.
Soil δ15N variations under different petroleum pollution conditions with and without plants. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations (p < 0.05).
3.2
δ13C and δ15N variation in plants under different petroleum pollution concentration
The δ13C values of Trifolium repens changed from −29.8‰ to −31.6‰, with an average of −30.5‰ (Fig. 4). A decreasing linear trend of the δ13C values was observed with increased petroleum contamination, where Trifolium repens was planted. The δ13C values of Agropyron cristatum have smoothly changed Trifolium from −12.6‰ to −13.1‰, with an average of −12.9‰, and the lowest values appeared for Agropyron cristatum without petroleum-contaminated soil (Fig. 4). Statistical analysis showed a significant difference among the different petroleum conditions for the δ13C values of Agropyron cristatum (p < 0.05). However, multiple comparison results showed that only the control and 3000 mg/kg petroleum-contaminated conditions differed from the δ13C values of Agropyron cristatum. Except for petroleum-contaminated soil conditions, a decreased linear trend of δ13C values was observed in the Agropyron cristatum plantation as petroleum contamination increased. The δ13C values show that Trifolium repens and Agropyron cristatum are C3 and C4 photosynthetic plants, respectively [51].
Figure
4.
δ13C changes of Agropyron cristatum and Trifolium repens under different soil petroleum pollution conditions. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations (p < 0.05).
Under different petroleum-contaminated soil concentrations conditions, δ15N values of Agropyron cristatum changed (Fig. 5). The δ15N values of Agropyron cristatum varied, ranging from 3.8‰ to 8.5‰ with an average value of 5.4‰. Except for control conditions, the δ15N values of Agropyron cristatum decreased as petroleum-contaminated soil concentration increased. However, there was no statistical difference between δ15N values without petroleum-contaminated soil and 10000 mg/kg petroleum-contaminated soil with Agropyron cristatum. The δ15N values of Trifolium repens ranged from 0.8‰ to 5.6‰ with an average of 3.7‰. δ15N values of Trifolium repens were at the same level without petroleum-contaminated soil, and 3000 mg/kg petroleum entered into the soil. However, δ15N values of Trifolium repens changed significantly from 3000 to 10000 mg/kg of petroleum put into the soil (Fig. 5).
Figure
5.
δ15N changes of Agropyron cristatum and Trifolium repens under different soil petroleum pollution conditions. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations (p < 0.05).
In this study, we identified notable variations in δ13C and δ15N in plants and soil in 12 experimental quadrats exposed to different concentrations of petroleum-contaminated soil. The δ13C and δ15N values of the soil ranged from −23.6‰ to −26.8‰ and from 1.9‰ to 3.2‰, respectively. The δ13C and δ15N values of the C3 plant of Trifolium repens ranged from −29.8‰ to −31.6‰ and from 0.8‰ to 5.6‰, respectively. In contrast, the δ13C and δ15N values of the C4 plant Agropyron cristatum ranged from −12.6‰ to −13.1‰ and from 3.8‰ to 8.5‰, respectively. The δ13C values of plants and soil decreased with increasing petroleum concentration in the soil. However, as petroleum concentration in the soil increased, the δ15N values of the soil increased, but the δ15N values of plants decreased. Moreover, the δ13C and δ15N values of Trifolium repens and Agropyron cristatum differed under different soil petroleum concentrations.
The δ13C and δ15N values of soil organic matter correlate with soil organic matter decomposition and microbial processes[52]. When petroleum enters the soil, the carbon to nitrogen ratio increases, influencing the physical, chemical, and biological characteristics of the soil, such as soil porosity, permeability, and organic matter content[53]. Afterward, changes in microbial species and activities influence carbon assimilation and degradation in the soil and increase soil δ13C values[54]. Moreover, the large amount of different δ13C values of petroleum entering the soil is also the reason for soil δ13C values changes. In our study, the corresponding δ13C values decrease in the soil demonstrates that petroleum concentration induces these differences under control conditions. We applied the mixing model to calculate the initial δ13C values of the soil and petroleum compounds (Table 3). The δ13C values of the polluted soil decreased after one month of bioremediation. Presumably, the decreased δ13C values originated from microbial biomass production via the consumption of petroleum hydrocarbons and the production of organic acids via the partial oxidation of hydrocarbons[55, 56]. As the carbon chain length increases, the δ13C values of aliphatic petroleum hydrocarbons decrease with microbial oil degradation[57, 58]. Aromatic petroleum fractions show higher δ13C values than aliphatic hydrocarbons[57, 58]. Zyakun et al.[58] reported that the microbiota primarily consumed the C12−C18 aliphatic and aromatic hydrocarbon fractions in the petroleum-contaminated soil. Furthermore, degrading aromatic fractions in the soil increases the aliphatic hydrocarbon fractions and decreases the soil δ13C values[58]. The results of this study were consistent with these findings.
Table
3.
The calculated and determined values of petroleum-contaminated soil with or without plants; ∆ indicates the difference of δ13C values between original soil and soil after one month of plant-microbial co-remediation.
The plant also influences the soil δ13C values[59]. In this research, the δ13C values decreased when the Trifolium repens were planted, but lower δ13C values appeared when the Agropyron cristatum was planted. Usually, δ13C values of the C3 pathway plant range from −20‰ to −32‰, whereas those of C4 plants from −9‰ to −17‰[60]. The soil δ13C values were influenced by the percent of C3 or C4 plant remnants in the soils[49] and the soil microbial activity, such as microbial degradation reaction[32]. Consequently, the difference in soil δ13C values with plants in the soil comes from plant growth and soil microbial activity. Compared to the C4 plant, the lower δ13C values of Trifolium repens caused lower δ13C values of carbohydrates into the soil. They decreased the soil δ13C values, which can also be testified by the relatively smaller δ13C value change of the Agropyron cristatum plantation (Fig. 4). However, this conclusion still needs to be testified because there has no clear statistical analysis to support it. This may also be related to the short duration of our experiment.
The δ13C values of Trifolium repens decreased as the petroleum-contaminated soil concentration increased (Fig. 4). However, the δ13C values of the Agropyron cristatum increased higher than those of the control. Usually, the δ13C values of plants increase under stress conditions (drought, nutrient limitation, saline conditions, sulfide toxicity, high temperature, and humidity deficit)[61, 62]. The petroleum added to the soil reduces the soil porosity and gaseous exchange, which is toxic to plants and soil, and might be the same as the stress for a plant to uptake water, nutrients, and oxygen. In addition, petroleum entering the soil increases the soil organic carbon content. All of the reasons mentioned above stress the growth of plants and soil microorganisms. Thus, we can conclude that the increased δ13C values of Agropyron cristatum are a response to environmental stress[62]. However, the δ13C values decreased with increasing petroleum-contaminated soil concentrations for the Trifolium repens plantation, implying that this plant has higher adaptability to environmental stress. Trifolium repens is a leguminous plant that can fix nitrogen from the atmosphere. Therefore, although the increased soil carbon to nitrogen ratio stresses plant uptake of nitrogen from soil and soil microbial activities[63], the nitrogen fixation ability of Trifolium repens can ease petroleum contamination stress. When the nitrogen source comes from the air, the δ15N values of nitrogen are close to zero[64]. The δ15N values of Trifolium repens showed a decreasing tendency with increasing soil petroleum concentration, which may imply Trifolium repens increases its nitrogen fixation ability from the atmosphere to reduce the shortage of nitrogen from the soil. Moreover, the nitrogen fixation ability of Trifolium repens offsets nitrogen shortage for the plant itself and can even feed on soil microbes. This symbiotic relationship between nitrogen-fixing plants and soil microbes is a favorable condition for petroleum-contaminated soil.
In our experiment, only the nitrogen concentration was detected in the soil, and we did not detect the nitrogen from the petroleum used in the experiment. Thus, we can conclude that the nitrogen in the soil mainly originates from the sample soil and organic fertilizers. Laboratory analysis showed that the δ15N values of the organic fertilizer and sample soil were 3.8‰ and 2.2‰, respectively. The δ15N values increased with increasing petroleum-contaminated soil concentration under control conditions, implying that petroleum-contamination influences the soil microbial community and activity[65]. John et al. found that, compared with unpolluted soil, ammonium and nitrate concentrations decreased with increased oil pollution levels in a crude oil-contaminated wetland. Moreover, nitrite was not detected in the contaminated soil, probably due to a reduction in the number of nitrogen fixers. Nitrosomonas and Nitrobacter cannot grow well in oil-polluted soil[66]. Therefore, we cautiously speculate that changes in δ15N values occur because Nitrosomonas and Nitrobacter activity and quantity are influenced by petroleum-contaminated soil.
Plants change soil δ15N values under petroleum contamination conditions. Under the Agropyron cristatum planting condition, except for 3000 mg/kg petroleum contamination, the soil δ15N values tended to comply with the control condition. However, the values of δ15N were lower than that for the control condition, which may be due to the plant-microbial partnership. For example, in underwater or saline stress conditions, ammonium uptake by plants requires less water consumption[67, 68]. The higher values of soil δ15N under 3000 mg/kg petroleum contamination with the Agropyron cristatum planted imply that a moderate concentration of soil oil pollution promotes soil and plant activity[3, 69, 70]. In the present study, higher concentrations of petroleum inhibited plant growth. However, Trifolium repens has lower δ15N values than Agropyron cristatum, which implies that the nitrogen fixation system of Trifolium repens is activated during petroleum-contaminated soil.
5.
Conclusions
In this study, δ13C and δ15N of plants and soil samples with varied soil petroleum concentrations were identified by the stable isotope-ratio mass spectrometer. Our in-situ field experiment shows that both δ15N and δ13C can be used as indices to trace the response and effect of petroleum-contaminated soil on plants and soil. The petroleum added to the soil induced the values of soil δ13C to decrease and δ15N to increase. Trifolium repens, and Agropyron cristatum can affect the soil values of δ15N and δ13C. However, the values of δ15N and δ13C for Trifolium repens and Agropyron cristatum showed different results with and without petroleum-contaminated soil, reflecting changes in the metabolic system when plants face a stressful environment. Our results suggest that δ15N and δ13C are useful proxies for monitoring soil petroleum contamination and evaluating plant stress response. The limitation of this study is that we only measured the whole plant and soil δ13C and δ15N values and only once during soil bioremediation processes, which impedes further detection of the mechanisms of plant and soil reactions in petroleum-contaminated soil. Future research efforts should focus on the mechanisms of petroleum component transformation, nitrogen mineralization, uptake assimilation, and transfer from the soil to plants under petroleum-contaminated soil.
Acknowledgements
We thank Miss Jing Hu for her assistance in the laboratory. This work was supported by the Key Research and Development Program of Shaanxi Province (2020SF-425), the Open Research Fund of State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment, CAS (SKLLQG1623), the Open Research Fund of Key Laboratory of Subsurface of Hydrology and Ecological Effect in Arid Region (Chang’an University), Ministry of Education (300102299507), and the Natural Science Basic Research Program of Shaanxi (2021JQ-791).
Conflict of interest
The authors declare that they have no conflict of interest.
1S.
The δ15N values of the in-house standard. Five samples inserted one in-house standard to monitor the accuracy of the isotope-ratio mass spectrometer.
The authors declare that they have no conflict of interest.
Petroleum-contaminated soil induced the soil δ15N values to increase and δ13C values to decrease.
The characteristics of plants influence plant δ13C and δ15N values under petroleum-contaminated soil.
The δ13C and δ15N values are useful proxies for monitoring petroleum-contaminated soil and evaluating the response of plants to the stress of petroleum contamination.
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Figure
1.
The Trifolium repens (a) and Agropyron cristatum (b) were collected from the experimental field after one month of growth. 0, 3000, 7000, and 10000 in the picture means the petroleum contamination concentration in the soil increased from 0, 3000, 7000 to 10000 mg/kg, respectively.
Figure
2.
Soil δ13C variations under different petroleum pollution conditions with and without plants. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations ( p < 0.05).
Figure
3.
Soil δ15N variations under different petroleum pollution conditions with and without plants. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations (p < 0.05).
Figure
4.
δ13C changes of Agropyron cristatum and Trifolium repens under different soil petroleum pollution conditions. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations (p < 0.05).
Figure
5.
δ15N changes of Agropyron cristatum and Trifolium repens under different soil petroleum pollution conditions. Error bars indicate the standard deviation (n = 3). Different letters indicate significant differences among petroleum-contaminated soil concentrations (p < 0.05).
1S.
The δ15N values of the in-house standard. Five samples inserted one in-house standard to monitor the accuracy of the isotope-ratio mass spectrometer.
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Table
3.
The calculated and determined values of petroleum-contaminated soil with or without plants; ∆ indicates the difference of δ13C values between original soil and soil after one month of plant-microbial co-remediation.
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