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Article

Plant and Microorganism Combined Degradation of Bensulfuron Herbicide in Eight Different Agricultural Soils

by
Yanan Zhang
,
Xin Wang
*,
Wenrui Liu
and
Ling Ge
School of Environmental and Chemical Engineering, Shenyang University of Technology, Shenyang 110870, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(12), 2989; https://doi.org/10.3390/agronomy12122989
Submission received: 17 October 2022 / Revised: 14 November 2022 / Accepted: 23 November 2022 / Published: 28 November 2022
(This article belongs to the Special Issue Remediation of Heavy Metal/Organic Pollutant Contaminated Farmland)
Browse Figures
Versions Notes

Abstract

:
Sulfonylurea herbicides (SH) are widely used throughout the world. In this paper, the degradation of sulfonylurea herbicides (SH) in eight different agricultural soils was studied by exploring the synergism between microbial consortium (MC) and plants. In the experiment, chlorimuron with a concentration of 50 mg/L was used as the only carbon source to domesticate and prepare the MC. The degradation of six sulfonylurea herbicides was determined, among which bensulfuron (BN), due to its better degradation effects, was selected. The best degradation conditions of BN were determined as follows: pH 7, 20 °C, and BN concentration 20 mg/L, and after 20 days, the degradation rate of BN by MC reached 90.49%. The physical and chemical properties of eight different agricultural soils were compared, and the correlation between them and the degradation effect of BN was analyzed. When plants were combined with 3% MC to remediate BN-contaminated soil, it was beneficial to plant growth, and the degradation rate of BN was the highest (81%) after 25 days. In addition, the content of soil urease and soil catalase in the soil increased to 449 ug/g and 12.19 mmol/g after 25 days of combined remediation. The results showed an effective bioremediation strategy to restore agricultural soil contaminated by BN.

1. Introduction

Sulfonylurea herbicides are non-volatile weak acids, whose acidity mainly comes from the ionization of hydrogen atoms on the nitrogen atom connected to the sulfonyl group [1]. Generally, the pKa value is 3–5, and the vapor pressure does not exceed 1.33 × 10−8 Pa [2,3]. Sulfonylurea compounds are easily hydrolyzed, and the hydrolysates of different compounds are also different and change accordingly with the change in pH. Sulfonylurea compounds mainly exist in the molecular form under acidic conditions, at which time the sulfonylurea bridge mainly undergoes a hydrolysis reaction to replace amino heterocycles and sulfonamide molecules [3,4]. However, under weak acid conditions, it exists in the form of negative ions. When the sulfonylurea compound is in a strongly alkaline environment, the hydrogen atom on the other nitrogen atom of the sulfonylurea bridge will be ionized. At this time, the hydrolysis of certain ester bonds of the aromatic ring and the nucleophilic substitution of alkoxy groups on the heterocyclic ring mainly occur [4,5]. A review by Sarmah et al. [6] shows that sulfonylurea hydrolyzes faster under acidic conditions (pH 4–7), while in alkaline agricultural soils it may be very slow. Data from other countries indicate that the half-life of sulfonylurea increases exponentially with pH and is also affected by changes in agricultural soil temperature and water content [7].
Sulfonylurea herbicides, when absorbed into plants, promote the production of acetolactate synthase (ALS) in plants, thereby inhibiting the production of leucine, isoleucine, amino acids, valine, and other substances, hindering plant roots and short tip growth [4,8,9,10,11]. They can be used to prevent and remove various broad-leaved weeds and gramineous weeds in cereal and other oil crop fields [12,13]. They are one of the most widely used herbicides at home and abroad. This is due to their low toxicity, high efficiency, high activity, and strong selectivity. They exhibit excellent herbicidal activity at very low doses, which is 100–1000 times that of traditional herbicides [10]. Sulfonylurea herbicides suitable for controlling weeds in various crops can be found.
However, the environmental risks caused by sulfonylurea herbicides present potential environmental problems. Sulfonylurea herbicides have a low vapor pressure and rarely evaporate into the atmosphere. The main way for them to enter the environment is to be absorbed by plants and enter the soil [14]. Some herbicides remain in the soil, causing phytotoxicity to sensitive crops planted later and affecting the growth of crops [15,16,17,18]. It may have some residues in soybeans, rice, and corn [19] and has a certain biological enrichment. Some studies have found that at pH 5.0, the maximum bioconcentration factor of chlorsulfuron in Chlorella is 53 [20]. Herbicide residues were found in citrus fruits (peeled grapefruit, lemon, and citrus) and vegetables (cucumber, eggplant, tomato, and zucchini) grown in the Jordan Valley, including bensulfuron-methyl residue. The irrigation water and soil at each planting site were relatively high in bensulfuron-methyl residue [21]. Other scholars have discovered that a kind of tree in Brazil is highly sensitive to sulfonylurea pesticides [22]. Studies in other countries have shown that under greenhouse and field conditions, herbicides can greatly delay flowering and reduce the yield of many species [23]. Like other chemical pesticides, sulfonylurea herbicides can easily penetrate into the surface and underground together with precipitation. Pesticides in the soil penetrate the groundwater together with surface runoff through the action of leaching or penetration into the soil layer, thus causing a certain degree of pollution to the groundwater [24].
The biodegradation of pesticides by microorganisms is a good treatment method [25], especially in weakly alkaline environments [26]. In recent years, scholars at home and abroad have conducted extensive research to study the degradation of sulfonylurea herbicides with complex structures that are difficult to degrade [27,28,29,30,31,32]. Through experiments, it was found that under normal circumstances, the degradation effect of a composite bacterial system on pollutants is much better than that of a single strain, and the degradation time can be greatly shortened [33]. In agricultural soil, microorganisms degrading sulfonylurea herbicides mainly include bacteria, actinomycetes, and fungi [31,34,35]. They degrade sulfonylurea herbicides mainly through co-metabolism, hydrolysis, and photolysis [36]. The main characteristics of the co-metabolism process can be summarized as follows: (A) microorganisms use a substance in the herbicide as a carbon source or other energy sources; (B) microorganisms consume pesticides as the second nutrient for energy supply; and (C) multiple enzymes participate together, and the key enzymes of different microorganisms are similar and can degrade the same kind of herbicide [37]. In order to accelerate the process of chemical hydrolysis, microorganisms will first select the hydrolysate of complex substances to carry out chemical reactions. For example, some sulfonylurea herbicides are mainly hydrolyzed in the reaction medium to produce intermediate hydrolysates, and then the microorganisms will biochemically react with the substances produced after hydrolysis to achieve the purpose of degrading the herbicides [29]. Boschin et al. [38] showed that under strictly controlled indoor chemical degradation conditions, the main intermediate metabolite in the process of degradation of chlorsulfuron and carboxamide by Aspergillus niger was obtained during the hydrolysis of the sulfonylurea bridge.
The products of pesticides metabolized by plants, microorganisms, and animals in soil were analyzed by liquid chromatography–mass spectrometry (LC–MS) [39].
The removal efficiency of microbial herbicides is affected by soil pH, temperature, and an appropriate initial herbicide concentration. The stronger the acidity of the soil, the higher the adsorption rate and the more disadvantageous the degradation. The rate of microbial degradation of these herbicides will also increase with increasing the temperature [40]. The main purpose of this study was to study the degradation effect of combined bacteria on sulfonylurea herbicides. From the initial concentration of herbicide, pH, and temperature, the influence of environmental factors on the degradation efficiency was studied. Finally, the best degradation conditions were determined, the best plan was put forward, and an agricultural soil simulation experiment was carried out.

2. Materials and Methods

2.1. Chemicals, Microorganisms, and Culture Medium

The microbial consortium (MC) and sulfonylurea herbicides (SH) used in the experiment were provided by the Shenyang Institute of Applied Ecology, Chinese Academy of Sciences.
The SH used were flucarbazone-sodium (FS, (sodium,(3-methoxy-4-methyl-5-oxo-1,2,4-triazole-1-carbonyl)-[2-(trifluoromethoxy)phenyl]sulfonylazanide), bensulfuron (BN, 2-({[(4,6-dimethoxypyrimidin-2-yl)carbamoyl]sulfamoyl}methyl)benzoic acid), foramsulfuron (FN, 2-[(4,6-dimethoxypyrimidin-2-yl)carbamoylsulfamoyl]-4-formamido-N,N-dimethylbenzamide), triflusulfuron (TN, 2-[4-dimethylamino-6-(2,2,2-trifluoroethoxy)-1,3,5-triazin-2-ylcarbamoylsulfamoyl]-m-toluic acid), tribenuron-methyl (TM, methyl 2-[[(4-methoxy-6-methyl-1,3,5-triazin-2-yl)-methylcarbamoyl]sulfamoyl]benzoate), and azimsulfuron (AN, 1-(4,6-dimethoxypyrimidin-2-yl)-3-[2-methyl-4-(2-methyltetrazol-5-yl)pyrazol-3-yl]sulfonylurea).
The inorganic salt medium (ISM) (g/L) used was as follows: 0.50 g NaNO3, 1.0 g (NH4)2SO4, 2.5 g Na2HPO4, 1.0 g KH2PO4, 0.108 mg Al2(SO4)3·18H2O, 0.28 mg KBr, LiCl, Na2MoO4·2H2O, Na2WO4·2H2O, and SnCl2·2H2O, 0.34 mg ZnSO4·H2O, 0.389 mg MnCl2·4H2O, 0.58 mg NiCl2·6H2O, 0.56 mg CoSO4·7H2O, KI, and CuSO4·5H2O, 0.611 mg H3BO3, and 300 mg FeSO4·7H2O and it was adjusted to pH = 7.0. After sterilization at 121 °C for 20 min and cooling to room temperature, 1 mL of vitamin solution and calcium magnesium solution filtered through filter membrane (0.22 µm) was added.
The vitamin solution (1 L) was composed of 200 mg para-aminobenzoic acid, 200 mg biotin, 200 mg folic acid, 200 mg nicotinic acid, 100 mg calcium pantothenate, 100 mg pyridoxine hydrochloride, 100 mg riboflavin, 100 mg vegetarian thiamine, and 1 mg of vitamin B12.
The calcium–magnesium solution (1 L) was composed of 30 g CaCl2 and 20 g MgCl2.

2.2. Agricultural Soil Samples

Eight agricultural soil samples of different textures were taken from diverse provinces of China (Table 1), which had never been treated with SH, from the agricultural soil surface (5–15 cm depth). Physical and chemical properties of the agricultural soils were studied and analyzed.

2.3. Inoculum Formulation

In order to obtain appropriate inocula, the MC was individually pre-cultured in a beaker flask containing 100 mL of ISM at 20 °C and shaken (160 rpm) for 20 d. Then, with an inoculation volume of 10%, it was cultured under the same conditions until the third generation.

2.4. Biodegradation of Pesticides in Liquid Medium

The MC obtained as described above was inoculated in a 250 mL Erlenmeyer flask containing 100 mL of ISM contaminated with FS, BN, FN, TN, TM, or AN (50 mg/L). The cultures were incubated at 20 °C under constant agitation (160 rpm) for 20 days, and the procedure was carried out with a control of pesticides contaminated with or without MC inoculation, and then three parallel experiments were repeated.
After 20 days, the degradation rate was measured and calculated, and the one with better degradation effects was selected for further study. The influencing factors were the initial concentration (30–70 mg/L, interval 10 mg/L), pH (5–9, interval 1), and temperature (10–30 °C, interval 5 °C) of herbicide, and these were selected to study their effects on the degradation efficiency and finally determine the best degradation conditions.

2.5. Biodegradation of BN in Different Types of Soils

The agricultural soil samples (T1-8) were air-dried and passed through a 5 mm sieve and were contaminated with appropriate stock solutions of BN (final concentration 2 mg/kg soil). Culture dishes were filled with 50 g of contaminated soil at 40% moisture (dry weight basis) and kept for 36 h at 25 °C so that water equilibrated in the agricultural soil. Then, the microcosms were inoculated with the MC (1.5 mL) obtained as described above and incubated at simulated natural conditions (22 °C, 8 h; 28 °C, 16 h) for 20 days. Soil samples were completely dried by a freeze dryer and were taken for residual pesticide concentration measurement (5 g).

2.6. Biodegradation of BN in Sterile and Non-Sterile Soil

In order to ensure the simulated contaminated soil fertility, T7 and T8 soil samples were mixed (1:2). For sterile soil microcosms, the materials were sterilized three times by autoclaving for 20 min at 121 °C, and 100 g of agricultural soil material was weighed in a pot and supplemented with BN solution to achieve a final concentration of 2 mg/kg. After solvent evaporation, the agricultural soil was treated with the MC at 3%, mixed thoroughly, and incubated in a thermostatic chamber at 25 °C in the dark. A set that had not been inoculated with MC was treated as a control. Samples were periodically removed for the determination of residual BN. Each treatment was performed in triplicate.

2.7. Combined Phytoremediation of Residual BN in Agricultural Soil

Dolichos lablab (DL), a Gramineae crop, was chosen as a remediation plant to cooperate with MC to jointly degrade BN to minimize the adverse effects of the residual BN on rotational crops. Non-sterile simulated agricultural soil was prepared as per Section 2.6. Meanwhile, seeds with good shapes and similar sizes were soaked in 1% H2O2 solution for 30 min and then soaked in deionized water for 6 h, placed on filter gauze wetted with deionized water and incubated (28 °C) for germination. Five vigorous seeds were planted in each flowerpot (diameter, 10 cm; height, 10 cm). The flowerpots were then placed in a light growth chamber (GPX-250, Hu’nan Xiangyi Laboratory Instrument Development Co., Ltd., Hu’nan, China) at 28/22 °C (day/night) under a 16/8 h light/dark cycle with 70% humidity. Flowerpots were irrigated with sufficient distilled water every two days (if necessary). On day 20 after treatment, the plants were harvested for the measurement of morphometric indices such as plant height and weight. To explore the effects of combined phytoremediation on the growth of DL and the degradation of BN, the experimental arrangement shown in Table 2 was carried out, and each treatment was repeated five times. In order to determine the contents of catalase, urease, and malondialdehyde in the soil, a kit from Beijing Box Shenggong Technology Co., Ltd. was used.

2.8. Analytical Method

For determining residual BN concentration from the liquid culture (5 mL), a fixed volume of 5 mL chromatographically pure acetonitrile was used, and the sample was allowed to completely dissolve for30 min. For determining the residual BN concentration from the soil, an extraction technique was performed. A total of 5 g of soil was transferred to centrifuge tubes and mixed with water and acetonitrile in a relationship of 5:5 mL, respectively. At the same time, 4 g anhydrous magnesium sulfate, 1 g sodium chloride, 1 g trisodium citrate dihydrate, and 0.46 g disodium citrate hemihydrate were added and vortexed for 3 min with a vortexer to allow the mixture to homogenize. The two extraction methods were finally centrifuged (4000× g, 5 min), and the extracts obtained were filtered through a 0.2 μm organic filter and analyzed by Agilent 1200 HPLC. The parameters of HPLC were column temperature: 40 °C; detection wavelength: 241 nm; mobile phase: acetonitrile: 1% aqueous acetic acid solution = 80:20 (v/v); and flow rate: 1.0 mL/min; injection volume: 20 μL.

2.9. Degradation Kinetics

The pseudo-first-order rate constant for the degradation of BN was determined by the integrated arrangement of the first order reaction kinetics (Equation (1)):
lnCt = ln C0 − kt,
In the above equation, C0 is the BN concentration in the soil at the initial moment, Ct is the BN concentration in the soil at time t, k is the removal rate constant (d−1), and t is the removal time (d).
The half-life was determined by Equation 2:
T1/2 = 1/k·ln2,
In the above equation, k is the removal rate constant (d−1),

2.10. Statistical Analyses

All assays were conducted in triplicate, and the results were the average of them. One-way analysis of variance (ANOVA) was used to test the significant differences between the treatments in the liquid systems and agricultural soil. Tests were considered significantly different at p < 0.05. These statistical analyses were performed using professional versions of the SPSS 23 software, and the partial least-squares method and ridge regression method were used for regression analysis.

3. Results and Discussion

3.1. Analysis and Explanation of Biodegradation in Liquid Medium

When the MC was cultured in ISM supplemented with BN as the only carbon source, microbial growth was observed. The decrease in the concentration of BN in the inoculated MC compared to that of the non-inoculated sample was considered to be from microbial degradation. The HPLC analysis confirmed a substantial dissipation of the three pesticides (Figure 1). At the end of incubation, the removal of BN was observed (90). It was observed that less than 10% of the BN was degraded in the controls, so the removal of BN could be due to microbial activity and not only to physicochemical factors. After 20 days, the degradation rates of BN, FN, FS, TN, TM, and AN were 90.0, 89.7, 73.8, 60.9, 33.5, and 9%, respectively. The degradation rate of BN was the most significant among the six herbicides. Therefore, this herbicide was taken as the research object of the subsequent influencing factors experiment.
To evaluate the influence of the initial BN concentration on its biodegradation by MC, experiments were conducted in ISM (pH 7.0; 30 °C) spiked with BN at concentrations of 20, 30, 40, 50, and 60 mg/L (Figure 2a). BN was degraded by 99.5%, 98%, 95%, 90%, and 75%, respectively, after being incubated for 20 d, and the corresponding average degradation rates were 0.99, 1.47, 1.9, 2.25, and 2.25 mg/L/d, respectively. Li Debin showed in their research results that strain L3 was used to degrade chlorimuron-ethyl [41]. The results showed that with the increase in the initial concentration of chlorimuron-ethyl, the degradation rate decreased. When the initial concentration was 10 mg/L, the degradation rate could reach 100%. When the initial concentration of the herbicide reached 20 mg/L, the degradation rate dropped to 90%. Similarly, Guo Jian’s experimental research showed that when the initial concentration of chlorimuron-ethyl was 20 mg/L, the degradation rate of chlorimuron-ethyl was the highest, reaching more than 90% [42]. However, when the initial concentration of chlorimuron-ethyl was increased to 100 mg/L and 200 mg/L, the degradation rate decreased significantly, reaching about 80%.
To test the influence of temperature on BN biodegradation by the MC, the temperature was increased from 10 to 30 °C (Figure 2b). After a 20 d incubation, the natural degradation of the BN in the control group was less than 9.0%. With the introduction of the MC into the medium, approximately 68.7%, 89.5%, and 37.8% of the BN was degraded at 15 °C, 20 °C, and 25 °C, respectively. However, no significant degradation was detected at 10 °C and 30 °C, with the degradation at these temperatures <20%, which was similar to that of the controls. In the low-temperature environments, the degradation rate of the herbicide was higher than that in the high-temperature environments, indicating that the composite bacterial system was suitable for repair in a low-temperature environment. This may be related to the growth of complex bacterial systems and the optimal temperature of enzymes in the bacterial system that effect herbicide degradation.
The effect of different pH values on the degradation of 50 mg/L of BN by the MC is presented in Figure 2c. The abiotic degradation efficiencies of BN were <8% in all the un-inoculated controls. In the inoculated samples, approximately 19.5%, 23.08%, 90.49%, 12.39%, and 9.41% of the BN was degraded at pH values of 5.0, 6.0, 7.0, 8.0, and 9.0, respectively, after incubation for 20 d at 20 °C in the dark (Figure 2c). When the pH value was 7.0, the degradation of BN by MC was significantly higher than that of the other experimental groups. This result suggested that the degradation of the BN was a pH-dependent process with an optimal pH of approximately 7.0. We determined the following explanations for the different degradations under alkaline and acidic conditions: the SH were easily hydrolyzed [3], and they hydrolyzed faster under acidic conditions (pH 4–7) [6].
The degradation dynamics of BN in ISM is shown in Figure 2d. The disappearance pattern of BN was found to follow first-order kinetics at the concentration of 50 mg/L. A total of <10% of the initially added BN disappeared without the inoculation of MC. In contrast, the half-life of the group along with the MC was about 18 days. After adding the MC, the degradation rate of the BN increased linearly with the increase in the culture time, and the degradation process basically reached equilibrium within 20 days. In our experiment, the correlation coefficient values (R2 = 0.988; Table 3) indicated that the experimental values could approach the theoretical values calculated from the first-order kinetics. Upon introduction, the MC quickly adapted to the environment and increased the degradation of fomesafen, demonstrating bioremediation potential for the elimination of the herbicide in ISM.

3.2. Soil Properties

Table 4 lists the physicochemical characteristics of the agricultural soils in eight different regions of China and analyzes the remediation effects of MC in BN-contaminated soils. The effects of diverse agricultural soil characteristics on pesticide biodegradation were assessed. The soils in the current experiment displayed a neutral to alkaline trend, with only two agricultural soils exhibiting a slightly acidic pH. A basic pH of agricultural soil facilitates the accruing of a higher concentration of salt, which affects the soil matrix causing capriciousness, which has a detrimental impact on it.
According to the physicochemical characterization, agricultural soil 1 possessed the lowest pH (4.96), while the highest pH value was found in agricultural soil 5 (8.26). An opposite trend for organic content (OC) was observed in these agricultural soils, with agricultural soil 1 showing the smallest OC (0.31%) and agricultural soil 5 displaying the largest OC (2.72%). This may have seriously affected the activity of the MC, which could be one of the reasons for the low degradation of agricultural soils 1 and 2 (<20%). In agricultural soils 4, 5, and 7, the degradation amounts were 64%, 59%, and 61%, respectively, which were similar to the value of 54% obtained in laboratory mud results.
The correlation between the basic physical and chemical properties of agricultural soil pH, OC, total salt, clay, silt, and sand and the degradation of BN by the MC was visually analyzed (Figure 3). The degradation of BN was observed to be influenced by the agricultural soils’ physicochemical properties. It was positively correlated with pH, OC, total salt content, and silt, and the R2 value was 0.6772, 0.0160, 0.0218, and 0.0445, respectively, and was negatively correlated with the clay and sand content (R2 = 0.0691 and 0.0436).
The difference in total salt content can affect the microbial community and function of soil. Some studies have found that an increase of total salt content will reduce the microbial diversity in soil and affect the number of functional microorganisms [43]. From the point of view of particle size, the smaller the particle size, the lower the number of bacteria, thus reducing competition between indigenous microorganisms [44].
These properties were related, so the partial least-squares method was used to establish a regression model between the agricultural soil physical and chemical properties and BN degradation. The pH was set as X1, total salt as X2, OC as X3, clay as X4, silt as X5, sand as X6, and the degradation as Y. The model obtained was Y = 1.139 X1 − 0.282 X2 + 0.075 X3 + 0.060 X4 − 0.232 X5 − 0.368 X6 (p < 0.05). The value of R2 indicated that these six properties influenced 82% of the degradation of BN.
After the predicted value of the above model and the actual value were verified by the chi-square test, there was no significant difference between them, and the determination coefficient of the model was 0.751. Therefore, the improved least-squares method could explain the effect of the soil physical and chemical properties on the degradation rate, and the predicted value was close to the actual value.

3.3. Combined Phytoremediation of Residual BN in Agricultural Soil

To assess the effect of both BN and MC on plants, growth parameters (GP) (stem length (SL), stem dry weight (SDW), and root dry weight (RDW)) were determined (Table 5). In the soil with added BN, SL was promoted, but there was significantly (p < 0.05) less RDW and SDW at a concentration of 2 mg/kg as compared to the control without BN. When 3% MC was inoculated, the growth of DL was repaired compared with only adding pesticides. However, when this soil was inoculated with MC at 5 and 10% concentrations, respectively, DL growth was inhibited. The possible reason is that competition between the MC and indigenous microorganisms led to a reduction in microorganisms that promote plant growth, and the degradation of these treatments were 81, 80, and 76%, respectively. Considering the degradation and GP, we decided to use DL plus 3% MC for the subsequent remediation. The combination of the two accelerated the remediation efficiency of the BN.
The remediation of soil was investigated, and the agricultural soil enzymatic activities were determined (Table 6). BN has a certain inhibitory effect on S-CAT [45]. All the treatments promoted the recovery of S-CAT. This may be because there were strains in the MC that could use BN to produce S-CAT at the same time. The urease was also repaired, except for in the case of single-plant repair. It was found that the combined remediation significantly increased the activity of S-UR compared with the single remediation. Chlorosulfuron [46], which is also a sulfonylurea herbicide, will increase the content of S-CAT in the process of soil degradation due to the presence of microorganisms. However, differently from BN, chlorosulfuron had an obvious inhibitory effect on S-UR.

3.4. Composition Changes in MC before and after Degradation

High-throughput sequencing technology was used to determine the structure and composition of the consortium before and after degradation (Figure 4). The results showed that the MC used in this paper was stable and could be repaired and degraded many times. However, the ratio of each microorganism changed, which may be due to the differences in the external carbon sources, resulting in changes in the number of different strains of herbicides that could be used. That is, each carbon source had a corresponding dominant flora, and a herbicide (carbon source) was added so that the growth and reproduction of strains that consumed the carbon sources became dominant, and the number of strains increased. In addition, as can be seen from the figure, in the process of degrading sulfonylurea herbicides using a composite bacterial system, the dominant bacteria groups were mainly Pseudomonas, Achromobacter, Variovorax sp., Pseudoxanthomonas sp., Hhoeflea, and Aquamicrobium sp. The degradation species of BN were the same before and after the degradation, but the ratio changed. The dominant bacteria corresponding to BN accounted for the largest proportion, which were Pseudomonas, accounting for 30–40%, followed by Variovorax sp, with a degradation rate of more than 85%, indicating that the dominant bacteria played a key role. They still accounted for a large proportion of the degradation process.
Due to the complex composition and structure of MC systems, they are more susceptible to environmental factors and changes in species and numbers. Ai et al. [47] found that the degradation of cellulose by bacterial consortium led to the accumulation of organic acids, which lowered the pH. Under these acidic conditions, some bacteria cannot survive. However, because there were bacteria in the system that could degrade organic acids, it buffered the pH of the system, which greatly reduced the death number of bacteria and was conducive to the degradation of cellulose by the consortium.

4. Conclusions

The results showed that the MC could degrade the six sulfonylurea herbicides used in this experiment, indicating that it had a wide range of degradation effects and has broad application prospects. The combined microbial agents could play a synergistic role among the bacteria, make full use of the carbon sources, and improved the degradation effects. After repeated use of the MC, high-throughput sequencing was conducted, and it was found that the bacterial species remained basically unchanged and relatively stable. Compared with natural degradation, this study showed that after adding the MC, the degradation half-life of BN was greatly shortened. Dolichos lablab (DL) was grown in agricultural soil spiked with BN and inoculated with the MC. Although the MC had the potential to remove the BN from the polluted agricultural soil, the DL significantly enhanced the potential of the MC to decontaminate the polluted agricultural soil. It was concluded that a plant–bacteria partnership was an effective strategy for the remediation of BN-contaminated agricultural soil.

Author Contributions

Formal analysis, Y.Z.; methodology, Y.Z.; investigation, Y.Z.; writing—original draft, Y.Z.; funding acquisition, X.W.; supervision, X.W; validation, X.W.; software, X.W.; resources, W.L.; data curation, W.L.; conceptualization, W.L.; visualization, L.G.; writing—review & editing, L.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (No. 21976124) and (No. 31705515).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The author sincerely thanks the teachers and students for their excellent help during the experiment.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02989 g001 550
Figure 1. Determination of degradation rate of six SH. Note, CK: without MC. The letters a to f indicate data from large to small.
Figure 1. Determination of degradation rate of six SH. Note, CK: without MC. The letters a to f indicate data from large to small.
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Agronomy 12 02989 g002 550
Figure 2. Effect of concentration (a), pH (b), and temperature (c) on the degradation of BN by MC in the liquid medium, and degradation kinetics of BN at concentration of 50 mg/L (d). Note, CK: without MC. The letters a to e indicate data from large to small.
Figure 2. Effect of concentration (a), pH (b), and temperature (c) on the degradation of BN by MC in the liquid medium, and degradation kinetics of BN at concentration of 50 mg/L (d). Note, CK: without MC. The letters a to e indicate data from large to small.
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Agronomy 12 02989 g003 550
Figure 3. Correlation analysis between soil physicochemical properties and microbial degradation. The straight line in the figure is the fitting line of scattered data.
Figure 3. Correlation analysis between soil physicochemical properties and microbial degradation. The straight line in the figure is the fitting line of scattered data.
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Agronomy 12 02989 g004 550
Figure 4. Results of high-throughput sequencing. Note: (1) initial strain (containing a small amount of carbon source chlorimuron-ethyl); (2) the experimental group (adding bensulfuron-methyl).
Figure 4. Results of high-throughput sequencing. Note: (1) initial strain (containing a small amount of carbon source chlorimuron-ethyl); (2) the experimental group (adding bensulfuron-methyl).
Agronomy 12 02989 g004
Table
Table 1. Source of agricultural soil samples.
Table 1. Source of agricultural soil samples.
NumberSourceType
1Hengxian County, Nanning, Guangxi ProvinceBrick red soil, ball clay
2Lichuan County, Fuzhou, Jiangxi ProvinceRed soil, sandy clay loam
3Qingpu District, Huaian City, Jiangsu ProvinceRice soil, sandy loam
4Meishan City, Sichuan ProvincePurple soil, silty clay
5Qinxian County, Changzhi City, Shanxi ProvinceLoess, silty loam
6Tengzhou, Shandong ProvinceCinnamon soil, loam
7Shenyang, Liaoning ProvinceBrown loam, sandy loam
8Fusong County, Baishan City, Jilin ProvinceBlack soil, sandy loam
Table
Table 2. Combined phytoremediation experiment arrangement.
Table 2. Combined phytoremediation experiment arrangement.
NumberExperimental Arrangement
1BN (sterile)
2BN (non-sterile)
3BN + DL (non-sterile)
4BN + MC (non-sterile)
5BN + DL + MC (non-sterile)
Table
Table 3. Dynamics parameters of BN.
Table 3. Dynamics parameters of BN.
Kinetic EquationHalf-Life (d)K (×10−2)(d−1)
MC addedCt = 50·e−0.0383t18.103.83
CKCt = 50·e−0.0032t214.870.32
Table
Table 4. Physical and chemical properties of agricultural soil samples.
Table 4. Physical and chemical properties of agricultural soil samples.
NumberpHTotal Salt
(mSiemens/cm)		Organic Content (%)Clay
(g/kg)		Silt
(g/kg)		Sand
(g/kg)		Microbial Degradation (%)
14.960.070.31627.41237.69134.9020.00
24.960.020.84270.71107.70581.8214.00
38.140.241.15110.34263.70563.8948.00
47.310.030.21439.54405.7728.6364.00
58.260.412.72177.42540.04282.5459.00
67.940.221.57224.62476.09299.2939.00
77.900.111.67243.18127.63566.2961.00
87.230.503.55150.80328.88520.3233.00
Table
Table 5. Effect of 2 mg/kg BN and MC inoculation on stem length (SL), stem dry weight (SDW), and root dry weight (RDW) of DL.
Table 5. Effect of 2 mg/kg BN and MC inoculation on stem length (SL), stem dry weight (SDW), and root dry weight (RDW) of DL.
TreatmentsStem Length (cm)Stem Dry Weight (×10−2) (g)Root Dry Weight (×10−3) (g)
DL only32.1457.3085.38
DL + BN35.3547.6051.23
DL + BN + 3% MC35.4954.9664.20
DL + BN + 5% MC32.8549.4951.37
DL + BN + 10% MC32.8845.9748.90
Table
Table 6. Enzymatic activities in BN-contaminated agricultural soil after 25 days of different remediation methods: soil catalase (S-CAT), soil urease (S-UR).
Table 6. Enzymatic activities in BN-contaminated agricultural soil after 25 days of different remediation methods: soil catalase (S-CAT), soil urease (S-UR).
TreatmentDegradation (%)S-UR (ug/g)S-CAT (mmol/g)
Initial30.001388.0087.60
Add 3% MC61.001510.0093.20
Add DL57.301288.0082.12
Add DL and 3% MC79.001837.0099.79
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Zhang, Y.; Wang, X.; Liu, W.; Ge, L. Plant and Microorganism Combined Degradation of Bensulfuron Herbicide in Eight Different Agricultural Soils. Agronomy 2022, 12, 2989. https://doi.org/10.3390/agronomy12122989

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Zhang Y, Wang X, Liu W, Ge L. Plant and Microorganism Combined Degradation of Bensulfuron Herbicide in Eight Different Agricultural Soils. Agronomy. 2022; 12(12):2989. https://doi.org/10.3390/agronomy12122989

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Zhang, Yanan, Xin Wang, Wenrui Liu, and Ling Ge. 2022. "Plant and Microorganism Combined Degradation of Bensulfuron Herbicide in Eight Different Agricultural Soils" Agronomy 12, no. 12: 2989. https://doi.org/10.3390/agronomy12122989

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