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Article

Improvement of Saline–Alkali Soil and Straw Degradation Efficiency in Cold and Arid Areas Using Klebsiella sp. and Pseudomonas sp.

by
Xiaoyu Zhao
1,2,
Xiaofang Yu
1,*,
Julin Gao
1,*,
Jiawei Qu
1,
Qinggeer Borjigin
1,
Tiantian Meng
3 and
Dongbo Li
1
1
Inner Mongolia Autonomous Region Engineering Research Center for In-Situ Maize Stalk Returning Microbiology, Inner Mongolia Agricultural University, Huhehaote 010010, China
2
Institute of Maize Research, Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, Huhehaote 010031, China
3
College of Agronomy, Hebei Agricultural University, Baoding 071001, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(11), 2499; https://doi.org/10.3390/agronomy14112499
Submission received: 3 September 2024 / Revised: 21 October 2024 / Accepted: 21 October 2024 / Published: 25 October 2024
(This article belongs to the Section Agricultural Biosystem and Biological Engineering)
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Abstract

:
Corn straw is an important renewable resource, which could improve the quality of saline–alkali cultivated land. However, the slow decomposition of crop residues in cold, arid, and saline–alkali soils can lead to serious resource waste and ecological crises. The use of beneficial microorganisms with degradation functions could solve these problems. In this study, three types of saline–alkali soil with low, medium, and high salinity levels were used in the straw-returning experiment. The experiment was conducted with four treatments: GF2 (Klebsiella sp.), GF7 (Pseudomonas sp.), GF2+GF7, and CK (control without bacteria). Microbial characteristics, straw degradation efficiency, element release rate, and soil factors were compared, and random forest linear regression and partial least squares path modeling analysis methods were utilized. The results indicated that the degradation of bacterial metabolites, the efficiency of corn stover degradation, the efficiency of component degradation, and the release rates of elements (C, N, P, and K) initially increased and then decreased with the increase in salinity. At the maximum value of moderately saline–alkali soil, the effect of GF2+GF7 treatment was significantly better than that of other treatments (p < 0.05). Given the interactive effects of saline–alkali soil and microbial factors, the application of exogenous degrading bacteria could significantly increase soil enzyme activity and soil available nutrients, as well as regulate the salt–alkali ion balance in soil. The cation exchange capacity (9.13%, p < 0.01) was the primary driving force for the degradation rate of straw in saline–alkali soil with different degrees of salinization under the influence of exogenous degrading bacteria. Straw decomposition directly affected the soil chemical properties and indirectly affected soil enzyme activity. The results of this study would provide new strategies and insights into the utilization of microbial resources to promote straw degradation.

1. Introduction

Soil salinization is a major global agricultural problem. The saline–alkali land area in the world is about 960 million hectares, accounting for 64.20% of the total cultivated land area. It is increasing by 1.5 million hectares every year, seriously damaging and weakening soil’s productivity [1]. China has approximately 9.2 million hectares of saline–alkali land, accounting for 6.62% of the country’s cultivated land [2]. Inner Mongolia is an important grain reserve of China, and it has played an important role in ensuring the country’s food supply. Inner Mongolia has approximately 1.057 million hectares of saline–alkali land, constituting one of the most concentrated areas of saline–alkali soil in China [3]. Furthermore, frequent droughts and irrigation systems that were not properly managed have exacerbated soil salinization [4], thereby putting remarkable pressure on local food production [5]. Therefore, exploring effective measures for the prevention and scientific restoration of salinized soil is necessary. Expanding the area of cultivated land and improving its quality could have important implications for the development of agriculture in cold and arid regions with saline–alkaline soil.
Straw returning in situ can effectively improve soil salinization [6]. This approach has a low cost and reduced environmental pollution compared with other methods to improve salinization, and it is an effective measure to achieve green agriculture and sustainable development. However, the degradation efficiency of straw returning is highly related to soil microorganisms, soil enzyme activity, soil temperature, soil moisture, soil chemical characteristics, and soil saline–alkali ions [7]. In the northern arid and cold region, the slow degradation of straw that is returned to the field in winter because of low temperatures and drought seriously affects the planting and germination of crops in the following year. Furthermore, saline–alkali soil further complicates straw returning to the soil [8]. Given their degradation capabilities, beneficial microorganisms can be used to accelerate straw decomposition. Such microorganisms produce large amounts of extracellular polymeric substances (EPS, ACC, and IAA) to neutralize the salt and alkali ions in the soil environment, alleviate soil salinization, and promote the growth and development of crops [9,10,11]. Some studies have found that applying an exogenous composite microbial consortium during straw incorporation can alter the native microbial community structure, increase the diversity of dominant microbial populations, and maintain them in a stable state for a long time [12,13]. Wang et al. [14] reported that the addition of exogenous lignocellulose-degrading bacteria to the straw-returning process in cold regions resulted in the degradation of 80.53% of cellulose, 47.11% of hemicellulose, and 35.09% of lignin within 270 days. Gong et al. [15] conducted a straw-return experiment using corn straw-decomposing bacteria, with the SCG-F-II treatment achieving a straw-degradation efficiency of 66.37% after 119 days. The remarkable breakdown of the large molecular polysaccharide structure in straw components was primarily due to the fact that microorganisms secreted abundant biodegradable enzymes, which are involved in the degradation of straw lignocellulose [16,17]. Liu et al. [18] found that applying decomposing microorganisms to the soil after straw is returned accelerates nutrient release, thereby increasing the availability of soluble nutrients and soil enzyme activity in the soil. Borjigin et al. [19] applied compound strain GF-20 to improve the straw degradation efficiency by 18.70% in the cold and arid areas of northern China. Zhang et al. [20] also carried out multi-point verification experiments on straw returning combined with low-temperature straw degradation compound bacteria M44 in arid and cold areas of northern China. The results showed that the degradation rate of maize straw was 58.13–62.53%, which was 3.82–8.29 percentage points higher than that of the control. Therefore, the application of exogenous degrading microorganisms in the straw-returning process can accelerate the degradation of straw and cause changes in soil chemical properties [21,22]. However, few reports have been found on the effects of applying exogenous and highly efficient degrading microorganisms to saline–alkali soil in cold and arid areas on the degradation of straw and changes in soil properties, and the use of microorganisms that are resistant to low temperatures and salinity lacks theoretical support.
In this study, straw returning to soils with low, medium, and high salinity levels was investigated. Separately, the research team applied the low-temperature salt-tolerant straw GF2 (Klebsiella sp.) and GF7 (Pseudomonas sp.), selected by the team earlier, as well as the stable microbial consortium GF2+GF7 obtained by combining the two bacterial strains. The ecological relationship between straw degradation and soil factors was also investigated using combined analysis of random forest regression and the partial least squares path model (PLS-PM). This study aimed to evaluate the degradation efficiency of straw and its components under external application of degrading bacteria in low, medium, and high saline–alkali soils, as well as to reveal the interaction between crop residues and soil factors during decomposition. This study provides theoretical support for improving straw degradation and saline–alkali soil using beneficial microorganisms.

2. Materials and Methods

2.1. Test Location and Strain Origin

The experimental site was located in Baotou City, Inner Mongolia, China, and the cultivated land with low, medium, and high salinity levels under straw-returning treatment was selected. Baotou City (41°13′–43°36′ N, 113°26′–116°13′ E) in Inner Mongolia is on the Tumechuan Plain, which has a typical mid-temperate continental monsoon climate [23], with an average elevation of 1.1 km and a total area of 10,500 ha. The summer rainfall in this region was low, with an average annual rainfall of 185 mm. Low temperatures and drought were also observed in winter. The shallow groundwater level on the Tumechuan Plain, Inner Mongolia, led to solute enrichment, and secondary salinization was severe. The basic properties of saline–alkali soils are shown in Table 1.
In this study, Klebsiella (CGMCC no. 30279) and Pseudomonas (CGMCC no. 30277) were used as treatments GF2 and GF7, respectively. The specimens were conserved at the China General Microbial Culture Preservation Management Center (China, Beijing). This laboratory isolated and screened two bacterial strains from saline–alkali soil in a cold and arid area, which are highly efficient in degrading crop residues at low temperatures and are resistant to saline–alkali conditions. Furthermore, no antagonistic reaction was observed between GF2 and GF7. Moreover, GF2 and GF7 were mixed in a 1:1 ratio to form a stable combination. The bacteria were mixed with fillers (corn stover husk powder, starch, and bran) in a 1:4 ratio and fermented before being frozen and dried to prepare a dry powder inoculant with 7.5 billion CFU/g [24].

2.2. Experiment Design

The maize stalk was dried at 70 °C and cut into 1 cm × 1 cm squares. Next, 20 g of the maize stalk was placed into a gauze bag (25 cm × 35 cm, 5 mm aperture) and added with 20 g of soil to increase the contact area between straw and soil. The composition of corn stalk is shown in Table 1. This experiment was designed as a split-plot experiment, with the main plot consisting of three levels of saline soil: low (L), medium (M), and high (H). Four treatments were applied in the subplot: GF2 (Klebsiella sp.), GF7 (Pseudomonas sp.), GF2+GF7, and CK (no inoculation). After harvesting the corn, the nylon bags were placed in the soil at a depth of 25 cm. Then, a dry powder bactericide was quantitatively applied to the surface of the nylon bag and they were finally filled with soil. The same amount of inactivated bactericide was applied to the bactericide treatment, and each treatment was repeated seven times. A thermometer and a hygrometer were positioned to monitor the soil conditions (Supplementary Figure S1). The treatment duration period was 40 days. The straw was removed to determine the degradation rate of straw and its components. Soil samples were also collected around the straw to determine the enzyme activity, chemical characteristics, and salt and alkali ions.

2.3. Bacterial Characterization

Enzyme activity (FPA), cellulase activity (CMC), and xylanase activity (XYA) of a filter paper were determined by using the 3,5-dinitrosalicylic acid method. Laccase (Lac) was determined by using the ABTS method. Lignin peroxidase (Lip) was determined using the veratrol method. Manganese peroxidase (Mnp) was determined by DMP [25]. The enzyme solution to be tested was added into 100 mM propionate sodium malonate buffer and 10 mM manganese sulfate solution. The absorbance at 270 nm was quickly determined using a spectrophotometer (TAS-990, Persee, Shanghai, China) and the manganese peroxidase activity was calculated. The content of EPS was determined by using the Congo red AGAR method. The content of deaminase (ACC) was determined by using ketobutyric acid extraction.

2.4. Soil Factors

The content of alkaline protease (ALPT) and alkaline phosphatase (AKP) in the soil was determined by using ninhydrin colorimetry and the inorganic phosphorus content method, respectively. The sodium phenol–sodium hypochlorite colorimetric method was used to determine the content of urease (SUE) in the soil. In addition, soil cellulase (SCL) and soil sucrase (SSC) were determined by using 3,5-dinitrosalicylic acid colorimetry. Soil catalase (CAT) was determined by potassium permanganate titration [26]. Soil pH was measured by using a pH meter (PH-3C, REX, Shanghai, China). The content of total salt (TS) and total nitrogen (TN) in the soil was determined by using the mass method and semi-micro Kjeldahl method, respectively. Soil available nitrogen (AN) was determined by using the alkaline diffusion method. Soil available phosphorus (AP) was determined by sodium bicarbonate extraction using the molybdenum–antimony anticolorimetric method. Soil available potassium (AK) was determined using a flame photometer (6400-A, Shanghai Precision Instrument, Shanghai, China). Soil organic carbon (SOM) was determined by using the potassium dichromate volumetric method and external heating method. Soil cation exchange capacity (CEC) was determined by ammonium acetate centrifugation, and the content of CO32−, HCO3−, Cl−, and SO42− in the soil was determined by potentiometric titration. The level of Ca2+ and Mg2+ cations was determined by EDTA titration, and that of Na+ and K+ ions was determined by using the differential method (spectrophotometer, TAS-990, Persee, Shanghai, China) [27].

2.5. Straw Degradation and Straw Element Release

The degradation efficiency of corn straw was measured by using the drying weight-loss method. An experiment involving returning straw to the field and burying bags in low, middle, and high saline–alkali soil was carried out. The straw degradation rate was calculated by removing the straw after 40 days, clearing the soil around the corn straw, and drying it in an oven at 60 °C to a constant weight. After drying, the corn stover was pulverized through a 1 mm sieve. The sieved stover was transferred to a special bag for neutralization and acid washing, and the cellulose and hemicellulose content were determined using a fiber analyzer (A200i, ANKOM, Shanghai, China) [14]. Lignin content was determined by washing the sample with 72% sulfuric acid and then ashing in a muffle furnace. The degradation efficiency of straw components was calculated on the basis of the loss of cellulose, hemicellulose, and lignin. The main elements in straw were determined, and the organic carbon content was determined by using the potassium dichromate volumetric method and external heating. The TN content was determined by H2SO4–H2O2 deboiling and distillation. The content of total phosphorus and total potassium was determined by using vanadium–molybdenum yellow colorimetry and flame spectrophotometry, respectively.

2.6. Statistical Analysis

The data in this article were collated and analyzed in Microsoft Excel 2021, and Origin 2021 was used for the plot. The SPSS (26.0) LDS test was used to test the significance of differences between treatments. The Fisher test was used to identify the main factors influencing soil and straw degradation efficiency among multiple groups. Using random forest (MSE) modeling [28], the importance of predictor variables was evaluated by assessing the decrease in prediction accuracy. The importance and statistical significance of each predictor variable were also determined using the “frPermute” package in R software (4.4.3). The importance of the model and the R2 value from cross-validation were responded to by using the “A3” package and by evaluating the 1000 permutations of the response variable. A structural equation model (PLS-PM) was used to investigate the direct and indirect factors affecting the degradation efficiency of straw. The path coefficient represented the direction and strength of the linear relationship among potential variables [29], and R2 represented the percentage of variables explained by other variables. PLS-PM was built using the “plspm” package in R software.

3. Results

3.1. Characterization of Degrading Bacteria

As shown in Figure 1, the content of filter paper enzyme, cellulose enzyme, xylanase, lacquer enzyme, Lip, and Mnp produced by the inoculum treatment initially increased and then decreased with the increase in salinity. The activities of the degrading enzymes reached the maximum in the medium saline–alkali condition. The GF2+GF7 treatment with different salinity levels was significantly higher than the other treatments (p < 0.05). The cellulase-degrading activity (FPA and CMC) of single-strain GF2 was significantly higher than that of GF7. Meanwhile, the degradation of lignin enzyme activity (Lac, Lip, and Mnp) was significantly higher in GF7 than in GF2. Therefore, single-strain GF2 had a strong metabolic degradation ability for cellulase, whereas GF7 had a strong metabolic degradation ability for ligninase, and their combination could achieve the maximum enzyme activity for degradation. Degrading bacteria could not only metabolize straw-degrading enzymes, but also produce EPS and deaminase (ACC). The production of EPS, ACC, and lignocellulose-degrading enzymes by applying microorganisms to different saline–alkali conditions showed consistent trends, with the maximum value occurring under medium saline–alkali conditions. The GF2+GF7 combination was significantly higher than that of other treatments (p < 0.05). Under medium salt–alkali conditions, EPS and ACC produced by GF2+GF7 increased by 66.01 g/L and 0.035 U/mg, respectively, compared with CK. Therefore, saline–alkali factors had significant effects on the enzyme activity of FPA, Lac, and Mnp (p < 0.01). Microbial factors also had significant effects on the content of CMC, XYA, Lip, EPS, and ACC (p < 0.01). The interaction among these factors significantly affected the degradation of enzymes, EPS, and ACC (p < 0.01).

3.2. Degradation of Straw and Its Components

After applying degrading bacteria to different degrees of saline–alkali soil for 40 days, the degradation efficiency of straw and its components initially increased and then decreased as the degree of saline–alkali conditions increased (Figure 2). The degradation efficiency of straw in medium saline–alkali soil reached the maximum. At the same saline–alkali level, the degradation efficiency of cellulose and hemicellulose by exogenous degrading bacteria was significantly higher than that of CK (p < 0.05). Of the treatments, GF2+GF7 showed the most significant increase, accounting for 17.11 percentage points compared with the control in the moderately saline–alkali soil (p < 0.05). GF2 significantly degraded cellulose and hemicellulose in saline–alkali soils of different degrees, and strain GF7 significantly degraded lignin. In low, medium, and high saline–alkali soils, the composite microbial combination GF2+GF7 significantly degraded cellulose, hemicellulose, and lignin compared with other treatments, and the degradation efficiency reached its maximum in moderately saline–alkali conditions, increasing by 17.11, 14.50, and 22.26 percentage points compared with the CK. The internal structure of the straw degraded by each treatment was observed using an electron microscope (Figure 3). We found that the internal structure of hemicellulose, cellulose, and lignin in the straw degraded by the external application of degrading bacteria was irregular, rough, and fragmented, with a lot of holes, which significantly improved its degradation efficiency. In medium saline–alkali soil, the highest number of bacteria reproduced, and the greatest degree of structural damage occurred. Notably, the treatment effects of GF2+GF7 are the most significant, which is consistent with the metabolic degradation enzyme pattern of bacteria.

3.3. Release Rate of Straw Elements

The release of carbon, nitrogen, phosphorus, and potassium from the straw was analyzed after the application of exogenous degrading bacteria for 40 days (Figure 4). The release of elements initially increased and then decreased with the increase in salinity, and GF2+GF7 was significantly higher in low, medium, and high saline–alkali soils than in other treatments (p < 0.05). In medium saline–alkali soil, the GF2+GF7 treatment had the largest increase in carbon, nitrogen, and phosphorus content compared with CK (p < 0.05), which increased by 14.90, 14.53, 11.12, and 13.77 percentage points, respectively. Therefore, saline–alkali factors had significant effects on CAR, NTR, PHR, and PTR (p < 0.05). In addition, microbial factors had a significant effect on PHR (p < 0.01). The interactive effects between saline–alkali factors and microbial factors have a significant impact on the release rate of all elements, reaching a highly significant level (p < 0.01). The linear regression of different inoculum treatments with regard to low, medium, and high salinity levels (Table 2) is consistent with the one-variable linear regression equation model (Yt = A + Bx).
Yt represents the release rate of straw elements and B represents the regression coefficient in the formula. All treatments showed that the rates of carbon, nitrogen, phosphorus, and potassium released from straw decreased with the increase in salinity level. The release of exogenous degrading bacterial elements initially increased and then decreased. Therefore, the regression coefficients of the treatment groups were significantly lower than those for CK, and significant differences were found between the treatment groups and CK (p < 0.05).

3.4. Soil Enzyme Activity

Soil enzyme activities could reflect soil health to a certain extent. The contents of ALPT increased with the increase in soil salinity, whereas those of AKP, SUE, SCL, SSC, and CAT decreased with the increase in soil salinity (Figure 5). Different degrees of saline–alkali soil showed a significant increase in AKP, SUE, SCL, SSC, and CAT content with the application of degrading bacteria, whereas ALPT content significantly decreased. Compared with CK, the GF2+GF7 treatment significantly decreased ALPT content (30.88%, p < 0.05) in the medium saline–alkali soil. In addition, the GF2+GF7 treatment significantly increased AKP, SUE, SCL, SSC, and CAT content compared with other treatments (p < 0.05). In medium saline–alkali soil, the increase in AKP, SUE, SCL, and CAT content under GF2+GF7 treatment was the largest compared with the control, accounting for 2.73 μmol/d/g, 466.35 μg/d/g, 3.43 mg/d/g, and 6.33 U/g, respectively (p < 0.05). Saline–alkali factors had significant effects on soil ALPT and AKP contents (p < 0.01). Microbiological factors had a significant impact on soil SUE, SSC, and CAT content (p < 0.01). The interaction between saline–alkali factors and microbial factors had a significant effect on all soil enzyme activities (p < 0.01).

3.5. Soil Chemical Properties

Given the secondary metabolites produced by microorganisms during their growth and reproduction, as well as the release of C, N, P, and K during straw degradation, the chemical properties of saline soil are changed (Table 3). With the increase in soil salinity, the pH level and content of TS and CEC increased, whereas the contents of TN, AN, AP, AK, and SOM decreased. The application of degrading bacteria significantly reduced the contents of TS and CEC in saline–alkali soil (p < 0.05), with GF2+GF7 having the greatest reduction. In low, medium, and high saline–alkali soils, the application of degrading bacteria significantly increased the contents of AN, AP, and SOM (p < 0.05). The external application of degrading bacteria compared with the CK treatment in different degrees of saline–alkali soils could reduce soil pH, TS and CEC content to a certain extent (p < 0.05). The effects of the external application of degrading bacteria on the pH level and content of TS and CEC in saline–alkali soils were not significant. Saline–alkali factors had significant effects on soil TS and CEC (p < 0.01). Microbiological factors had a significant impact on soil AN, AK, AP, and SOM (p < 0.01). Furthermore, the interaction between saline–alkali factors and microbial factors had significant effects on TN, AN, AK, AP, and SOM (p < 0.01).

3.6. Soil Salt and Alkali Ions

The effects of degrading microorganisms applied to different degrees of saline–alkali soil on soil saline–alkali ions were analyzed (Table 4). The results showed that the contents of Cl− and SO42− were significantly reduced by the application of degrading bacteria. Notably, the content of Cl− and SO42− ions was significantly lower in the GF2+GF7 treatment in low, medium, and high saline–alkali soils than that in the CK (p < 0.05), accounting for 0.37, 1.04, and 1.03 g/kg, as well as 0.31, 1.14, and 1.46 g/kg, respectively. The contents of HCO3−, CO32−, Ca2+, Mg2+, Na+, and K+ in soil were not significantly affected by the external application of degraded bacteria (p > 0.05). Saline–alkali factors had significant effects on soil saline–alkali ions (p < 0.05 and p < 0.01). In contrast, microbial factors significantly affected the content of Cl− and SO42− (p < 0.05). The interaction between saline–alkali and microbial factors had significant effects on Cl− and SO42− (p < 0.05 and p < 0.01).

3.7. Correlation Fitting Analysis between Straw Degradation and Soil Factors

As determined through random forest regression and Spearman correlation analysis (Figure 6), applying efficient degrading bacteria to different degrees of saline–alkali soil affects the maximum driving force of straw degradation, which is CEC (9.13%, p < 0.01), followed by Xya (6.49%, p < 0.01) and TS (6.34%, p < 0.01). NTR, EPS, CMC, ACC, and other key factors are also included in the analysis. The indicators that were significantly correlated with straw degradation rate (CEC, Xya, TS, NTR, EPS, and CMC) were analyzed by linear regression to compare the trends in straw degradation rate among different saline–alkali soil treatments (Figure 6b). The external application of degrading bacteria resulted in significant reductions in CEC and EPS, whereas no significant differences were observed in the untreated control. The GF2+GF7 treatment significantly increased Xya (R2 = 0.669), NRT (R2 = 0.695), TS (R2 = 0.587), and CMC (R2 = 0.609) with a significant reduction in straw degradation rate (p > 0.01). The CK test showed no significant differences among various indicators.

3.8. Key Factors Affecting Straw Degradation

Through PLS-PM, the potential pathways by which the application of microbial agents and soil factors affect straw decomposition were revealed (Figure 7), with the optimal fitting degree of the model being 0.887. Soil chemical properties directly affected the degradation efficiency of corn straw (78.93%). In contrast, soil enzyme activity indirectly affected the degradation efficiency of corn stalk (48.40%). The negative effect of soil saline and alkali ions on the efficiency of straw degradation was the largest (−0.763, p < 0.001). The positive effect of exogenous degrading bacteria on straw degradation efficiency was the largest (0.843, p < 0.001), followed by the elemental release rate (0.739, p < 0.001). The main factors affecting the chemical properties of soil were TS, AN, SOM, and CEC. The main factors affecting soil saline and alkali ions were SO42−, HCO3−, CO32−, and Cl−. The main factors affecting soil enzyme activity were SUE, ALPT, CAT, and SCL.

4. Discussion

Klebsiella and Pseudomonas are the most representative genera of Proteobacteria and are important sources of various key metabolites and carbohydrate-related hydrolytic enzymes [30,31,32]. Some scholars have found [33] that Klebsiella can multiply rapidly under high saline–alkali conditions and efficiently degrade straw cellulose and hemicellulose. Klebsiella can produce a large amount of cellulase and xylanase enzymes, which could break down the cellulose and hemicellulose structures of corn stalks, thereby causing straw peeling [33,34]. Shen et al. [35] showed that Pseudomonas had a significantly positive correlation with lignin degradation. It can grow normally at low-temperatures [20], and its metabolic products contain large amounts of lacquer enzyme, Mnp, and Lip to accelerate lignin degradation [36]. The results of this study revealed that the enzymatic degradation activity of Klebsiella and Pseudomonas metabolism initially increases and then decreases with the increase in soil salinity. In the medium saline–alkaline soil (pH 8.95, TS 5.22 g/kg), the enzyme activity reached its maximum value. Klebsiella exhibited rich metabolism in cellulase enzymes (FPA, CMC), whereas Pseudomonas showed a high metabolic activity in lignin-degrading enzymes (Lac, Lip, and Mnp), which is consistent with previous research findings [35]. Meanwhile, the study also found that Klebsiella and Pseudomonas produce a large amount of EPS and ACC. Extracellular polymers can neutralize salt and alkali ions in the soil, whereas deaminase can enhance the activity of soil carbon and nitrogen cycling-related enzymes. The production of degrading enzymes, EPS, and ACC was significantly higher in the GF2+GF7 treatment compared with other treatments (p < 0.05). These results indicated that low-temperature salt-tolerant bacteria could produce abundant lignocellulose-degrading enzymes, EPS, and ACC, thereby playing an important role in the efficient degradation of straw and improvement of saline–alkaline soil.
Previous studies have found that the degradation efficiency of straw mixed with degrading agents gradually decreases as the salinity and alkalinity increase [37]. The results of this study showed that the degradation of straw and its components and the release rate of elements (C, N, P, and K) in the low, medium and high saline–alkali soil showed a trend of first increasing and then decreasing, and the maximum value was reached in moderate salinity and alkalinity. Some studies have found that carbon in straw could be decomposed and transformed by degrading bacteria, part of which could be converted into stable soil humus and increase soil fertility [19]. Nitrogen released from straw could promote plant root development, stem and leaf growth, fruit ripening, and photosynthesis. Phosphorus released from straw was one of the essential elements for the growth and development of plants and microorganisms. The release of potassium from straw could enhance the resistance of plants to pests and diseases, reducing the damage to plants [20]. Previous studies confirmed that promoting straw decomposition through microbial degradation was an effective method to enhance the degradation rate, especially by adding a composite microbial system [38]. The results showed that the single-strain GF2 (Klebsiella) had remarkable degradability of cellulose and hemicellulose, and the variation ranges were 22.58–25.63% and 21.23–24.38%, respectively. Meanwhile, the GF7 (Pseudomonas) showed a significant degradation of lignin at 26.23–31.53%. The degradation effect of GF2+GF7 was significantly higher than the other treatments (p < 0.05). The efficiency of straw degradation in different degrees of saline–alkali soil ranged from 28.57% to 32.57%, cellulose degradation efficiency ranged from 23.45% to 27.29%, hemicellulose degradation efficiency ranged from 22.77% to 26.75%, and lignin degradation efficiency ranged from 28.58% to 32.83%. This was due to the capability of two non-antagonistic degrading bacteria to form a stable degrading bacteria combination and metabolize more abundant fiber lignin-degrading enzymes than single strains. Moreover, it could enhance the stability of its metabolic degradation enzyme activity and improve its growth adaptability in more harsh environments (Figure 8). The interaction between saline–alkali factors and microbial factors had a significant effect on the release rate of C, N, P, and K (p < 0.01). The use of scanning electron microscopy to detect the degradation ability of microorganisms also confirmed this conclusion. The external application of degrading bacteria resulted in an irregular, rough, and fragmented internal structure of straw with numerous cavities, severely damaging its structure [39,40]. This indicates that exogenous degrading bacteria can disrupt the stubborn structure inside straw, especially with significant effects on lignin degradation, and the microbial combination of GF2+GF7 is more effective in exerting degradation.
The degradation process of returning straw to the field is remarkably influenced by soil environment and quality, as well as factors such as soil temperature, humidity, salinity level, readily available nutrients, and enzyme activity [41,42,43]. The results indicated that the application of degrading bacteria significantly increased soil enzyme activities (AKP, SUE, SCL, SSC, CAT) compared with CK, with GF2+GF7 being the most effective treatment. But the activity of ALPT was significantly decreased. This result is consistent with that of previous studies [44,45,46]. Degrading bacteria can not only secrete organic acids, ACC, and other substances but can also increase the activity of enzymes involved in the carbon and nitrogen cycle in soil, thereby improving the decomposition effect of straw [47]. Some studies had found that soil alkaline protease (ALPT) is involved in the degradation and transformation of organic matter in soil [33]. Soil alkaline phosphatase (AKP) can catalyze the hydrolysis of organophosphorus compounds to provide necessary nutrients for plants. Soil urease (SUE) can hydrolyze urea in soil to ammonia and carbon dioxide and release nitrogen sources that can be absorbed and utilized by plants. Soil cellulase (SCL) is derived from soil microorganisms and promotes the circulation of organic matter and the improvement of soil fertility [48]. Soil sucrase (SSC) is an enzyme that catalyzes the hydrolysis of sucrose into glucose and fructose and provides a carbon source and energy for soil microorganisms. Soil catalase (CAT) can eliminate and mitigate the harm of hydrogen peroxide, maintain soil health, and promote plant growth [49]. This study found that the application of degrading bacteria significantly increased the content of AN, AP, AK, and SOM in the soil while effectively reducing TS and CEC levels (p < 0.05), with the GF2+GF7 treatment showing the best performance. Therefore, the degradation of straw remarkably increases the content of available nutrients such as C, N, P, and K in the soil. Meanwhile, Klebsiella and Pseudomonas metabolize a large number of extracellular polymers to neutralize soil salinity and reduce the degree of soil alkalinity [50]. Through MES and linear regression analysis, a study found that CEC (9.13%, p < 0.01) is the maximum driving force of straw degradation influenced by exogenous degrading bacteria in low, medium, and high saline–alkali soils [51], followed by Xya (6.49%, p < 0.01). Using PLS-PM [29] to simulate the possible pathways of straw degradation influenced by exogenous degrading bacteria and soil factors, the experimental results revealed that soil chemical properties directly affect the efficiency of maize straw degradation. In contrast, soil enzyme activity indirectly affects the efficiency of maize straw degradation. Therefore, exploring the degradation function of Klebsiella and Pseudomonas and constructing an efficient microbial community for straw returning in saline–alkali land in cold–arid areas are necessary to improve the quality of cultivated land (Figure 8).

5. Conclusions

Returning straw to the field is an agricultural measure to improve saline–alkali soil, which can reduce water loss and salt migration through straw mulching. In addition, the straw components are decomposed into available nutrients, improving the soil saline–alkali environment and enhancing the fertility of cultivated land. This study reports for the first time that applying Klebsiella and Pseudomonas in low, medium, and high saline–alkali soils of the Hetao Plain can improve the degradation efficiency of straw and enhance salt-affected soil health management. The addition of a combination of composite bacteria remarkably enhances the efficiency of straw degradation and promotes the release of its main elements. It also improves soil enzyme activity and soil available nutrients and reduces soil salinity. In addition, CEC is considered as the maximum driving factor affecting straw degradation in low, medium, and high saline–alkali soils. This study provides a scientific basis for the utilization of saline–alkali land in the Hetao Plain and novel insights into the potential mechanism of using beneficial microorganisms to improve saline–alkali land.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/agronomy14112499/s1, Supplementary Figure S1. Analysis of temperature and moisture changes in different degrees of saline–alkali and alkaline soils.

Author Contributions

X.Z. and D.L. performed the experiments. X.Z. and X.Y analyzed the data. X.Y., J.G., Q.B., J.Q. and T.M. revised the manuscript critically for important intellectual content. X.Z. and X.Y wrote the paper. All authors have read and agreed to the published version of the manuscript.

Funding

Funding was provided by the National Key Research and Development Program (2023YFD2301801, 2023YFD1501500-01), National Natural Science Foundation of China (32260532, 32060434), Inner Mongolia Natural Science Foundation of China (2024MS03052), Key Laboratory of Crop Cultivation and Genetic Improvement of Inner Mongolia Autonomous Region (2023KYPT0023), Special Project of Carbon Peak and Carbon Neutralization in Universities of Inner Mongolia Autonomous Region (STZX202304), Basic Scientific Research Fund of Universities directly under Inner Mongolia Autonomous Region (BR22-11-07), and National Technical System for Maize Industry (CARS-02-74).

Data Availability Statement

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

Acknowledgments

We appreciate all the people who collaborated on this project.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Analysis of the activity and saline–alkali resistance of different bacteria. L, M, and H denote low salt base, moderate salt base, and high salt base, respectively. S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level; ** indicates significance at 0.01 level. Lowercase letters indicate significance at p < 0.05.
Figure 1. Analysis of the activity and saline–alkali resistance of different bacteria. L, M, and H denote low salt base, moderate salt base, and high salt base, respectively. S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level; ** indicates significance at 0.01 level. Lowercase letters indicate significance at p < 0.05.
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Figure 2. Degradation efficiency of corn straw, cellulose, hemicellulose, and lignin in saline–alkali soil with degrading bacteria. (a) shows the low salt base (L), (b) shows the moderate salt base (M), (c) shows the high salt base (H). SDR, CDR, HDR, and LDR indicate the straw degradation efficiency, cellulose degradation efficiency, hemicellulose degradation efficiency, and lignin degradation efficiency, respectively. Lowercase letters indicate significance at p < 0.05.
Figure 2. Degradation efficiency of corn straw, cellulose, hemicellulose, and lignin in saline–alkali soil with degrading bacteria. (a) shows the low salt base (L), (b) shows the moderate salt base (M), (c) shows the high salt base (H). SDR, CDR, HDR, and LDR indicate the straw degradation efficiency, cellulose degradation efficiency, hemicellulose degradation efficiency, and lignin degradation efficiency, respectively. Lowercase letters indicate significance at p < 0.05.
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Figure 3. Using an electron microscope, the straw degradation rate of bacteria after being applied in the soil with different salinity levels for 40 days was observed. (a–c) show CK treatment in low, moderate and high saline-alkali soil; (d–f) show GF2 treatment in low, moderate and high saline-alkali soil; (g–i) show GF7 treatment in low, moderate and high saline-alkali soil; (j–l) show GF2+GF7 treatment in low, moderate and high saline-alkali soil.
Figure 3. Using an electron microscope, the straw degradation rate of bacteria after being applied in the soil with different salinity levels for 40 days was observed. (a–c) show CK treatment in low, moderate and high saline-alkali soil; (d–f) show GF2 treatment in low, moderate and high saline-alkali soil; (g–i) show GF7 treatment in low, moderate and high saline-alkali soil; (j–l) show GF2+GF7 treatment in low, moderate and high saline-alkali soil.
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Figure 4. Analysis of the release rate of elements after the application of degrading bacteria in different degrees of saline–alkali soil. (a) Straw carbon release rate (CAR), (b) straw nitrogen release rate (NTR), (c) straw phosphorus release rate (PHR), and (d) straw carbon release rate (PTR). S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level, and ** indicates significance at 0.01 level. Lowercase letters indicate significance at p < 0.05.
Figure 4. Analysis of the release rate of elements after the application of degrading bacteria in different degrees of saline–alkali soil. (a) Straw carbon release rate (CAR), (b) straw nitrogen release rate (NTR), (c) straw phosphorus release rate (PHR), and (d) straw carbon release rate (PTR). S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level, and ** indicates significance at 0.01 level. Lowercase letters indicate significance at p < 0.05.
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Figure 5. Changes in soil enzyme activity under different salinity levels applied exogenously. ALPT, AKP, SUE, SCL, SSC, and CAT refer to soil alkaline protease, soil alkaline phosphatase, soil urease, soil cellulase, soil invertase, and soil catalase, respectively. S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level; ** indicates significance at 0.01 level; and *** indicates significance at 0.001 water level. Lowercase letters indicate significance at p < 0.05.
Figure 5. Changes in soil enzyme activity under different salinity levels applied exogenously. ALPT, AKP, SUE, SCL, SSC, and CAT refer to soil alkaline protease, soil alkaline phosphatase, soil urease, soil cellulase, soil invertase, and soil catalase, respectively. S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level; ** indicates significance at 0.01 level; and *** indicates significance at 0.001 water level. Lowercase letters indicate significance at p < 0.05.
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Figure 6. Random forest regression and Spearman correlation analysis identified the key factors to improve the degradation efficiency of corn straw (a). Linear fitting analysis of the correlation between different treatment key factors and the degradation rate of straw (b). * indicates significance at 0.05 level, and ** indicates significance at 0.01 level.
Figure 6. Random forest regression and Spearman correlation analysis identified the key factors to improve the degradation efficiency of corn straw (a). Linear fitting analysis of the correlation between different treatment key factors and the degradation rate of straw (b). * indicates significance at 0.05 level, and ** indicates significance at 0.01 level.
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Agronomy 14 02499 g007
Figure 7. Effects of microbial treatment and soil factors on straw degradation using PLS-PM (a). The red and blue arrows represent positive and negative causal relationships, respectively, whereas the thickness of the lines indicates significance (thin for p < 0.05, medium for p < 0.01, and thick for p < 0.001). The numbers on the arrows indicate significant standardized path coefficients. R2 represents the variance explained by the model’s dependent variable. Effect analysis (Direct Effects, Indirect Effects and Total Effects) of microbial treatments and soil factors (b). ADM refers to microbial treatment; SPH represents soil chemical characteristics; SAI denotes soil salinity and alkalinity ions; SEA indicates soil enzyme activity; ERE indicates straw element release rate. * indicates significance at 0.05 level; ** indicates significance at 0.01 level; and *** indicates significance at 0.001 level.
Figure 7. Effects of microbial treatment and soil factors on straw degradation using PLS-PM (a). The red and blue arrows represent positive and negative causal relationships, respectively, whereas the thickness of the lines indicates significance (thin for p < 0.05, medium for p < 0.01, and thick for p < 0.001). The numbers on the arrows indicate significant standardized path coefficients. R2 represents the variance explained by the model’s dependent variable. Effect analysis (Direct Effects, Indirect Effects and Total Effects) of microbial treatments and soil factors (b). ADM refers to microbial treatment; SPH represents soil chemical characteristics; SAI denotes soil salinity and alkalinity ions; SEA indicates soil enzyme activity; ERE indicates straw element release rate. * indicates significance at 0.05 level; ** indicates significance at 0.01 level; and *** indicates significance at 0.001 level.
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Agronomy 14 02499 g008
Figure 8. Effects of applying low-temperature saline–alkali-tolerant and efficient straw-degrading bacteria on straw degradation and saline–alkali soil.
Figure 8. Effects of applying low-temperature saline–alkali-tolerant and efficient straw-degrading bacteria on straw degradation and saline–alkali soil.
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Table 1. Chemical properties of saline–alkali soil in different degrees and contents of corn stalk components.
Table 1. Chemical properties of saline–alkali soil in different degrees and contents of corn stalk components.
Saline–Alkali SoilpHTS (g/kg)CEC (cmol/kg)Maize StrawCellulose Content (%)Hemicellulose Content (%)Lignin Content (%)
Low level8.203.239.81Xianyu 69638.4428.1722.45
Middle level8.955.2215.26Xianyu 69638.4428.1722.45
High level9.217.8921.74Xianyu 69638.4428.1722.45
Table 2. Fitting between the release rate of degraded bacterial elements and the degree of saline–alkali in different saline–alkali soil applications.
Table 2. Fitting between the release rate of degraded bacterial elements and the degree of saline–alkali in different saline–alkali soil applications.
Element ReleaseHandleEquation Yt (%)Regression CoefficientR2
CarbonCKYt = −0.9854x + 6.2553−0.98540.9556
GF2Yt = −1.4556x + 14.9273−1.45560.6439
GF7Yt = −1.7971x + 14.5274−1.79710.6551
GF2+GF7Yt = −1.4456x + 19.7647−1.44560.7723
NitrogenCKYt = −0.4051x + 4.6933−0.40510.9815
GF2Yt = −0.4579x + 14.2278−0.45790.4018
GF7Yt = −0.5547x + 14.8259−0.55470.6218
GF2+GF7Yt = −0.1498x + 17.1836−0.14980.5047
PhosphorusCKYt = −0.1359x + 3.3973−0.13590.9631
GF2Yt = −0.9854x + 11.8773−0.98540.4249
GF7Yt = −1.1127x + 12.7891−1.11270.5033
GF2+GF7Yt = −0.9523x + 14.8415−0.95230.5297
PotassiumCKYt = −1.0025x + 10.1871−1.00250.9016
GF2Yt = −0.9854x + 18.2291−0.98540.4252
GF7Yt = −0.8854x + 19.0325−0.88540.5278
GF2+GF7Yt = −1.1653x + 23.1714−1.16530.5491
Table 3. Changes in the chemical properties of soil with different levels of salinity after the application of degrading bacteria.
Table 3. Changes in the chemical properties of soil with different levels of salinity after the application of degrading bacteria.
SalinityHandlepHTS
(g/kg)		TN
(g/kg)		AN
(mg/kg)		AP
(mg/kg)		AK
(mg/kg)		SOM
(g/kg)		CEC (cmol/kg)
LCK8.21 ± 0.05 b3.23 ± 0.06 e0.91 ± 0.05 b44.12 ± 0.15 c27.56 ± 0.26 c163.01 ± 4.15 c13.56 ± 0.26 c9.87 ± 0.15 f
GF28.15 ± 0.13 b2.37 ± 0.12 f1.01 ± 0.06 a45.23 ± 0.26 b31.36 ± 0.18 b181.23 ± 4.26 b14.79 ± 0.21 b8.55 ± 0.26 g
GF78.24 ± 0.24 b2.26 ± 0.11 f1.12 ± 0.06 a46.73 ± 0.31 b31.59 ± 0.09 b182.47 ± 3.26 b15.01 ± 0.15 b8.06 ± 0.15 g
GF2+GF78.07 ± 0.16 b2.24 ± 0.08 f1.31 ± 0.14 a50.11 ± 0.36 a32.61 ± 0.15 a191.26 ± 5.26 a16.29 ± 0.06 a7.09 ± 0.09 g
MCK8.95 ± 0.17 b5.22 ± 0.21 c0.63 ± 0.15 d31.56 ± 0.25 e24.15 ± 0.36 d138.26 ± 5.59 e7.18 ± 0.19 e15.26 ± 0.13 d
GF28.33 ± 0.16 b4.31 ± 0.23 d0.82 ± 0.08 c40.26 ± 0.31 d27.07 ± 0.28 c147.26 ± 3.98 d11.23 ± 0.26 d13.12 ± 0.15 e
GF78.36 ± 0.14 b4.23 ± 0.18 d0.84 ± 0.07 c41.31 ± 0.18 d26.87 ± 0.24 c146.26 ± 4.15 d11.59 ± 0.31 d13.36 ± 0.14 e
GF2+GF78.25 ± 0.14 b3.98 ± 0.31 d0.93 ± 0.08 b43.74 ± 0.37 c27.78 ± 0.26 c158.14 ± 5.12 c12.01 ± 0.15 c12.91 ± 0.17 e
HCK9.18 ± 0.25 a7.89 ± 0.26 a0.31 ± 0.14 e21.36 ± 0.28 g15.91 ± 0.31 g123.45 ± 5.06 f5.23 ± 0.26 f21.74 ± 0.19 a
GF29.01 ± 0.21 a6.39 ± 0.41 b0.41 ± 0.15 e28.31 ± 0.26 f19.23 ± 0.18 f133.26 ± 4.78 e6.11 ± 0.26 e18.58 ± 0.21 b
GF78.88 ± 0.15 b6.21 ± 0.13 b0.39 ± 0.06 e28.91 ± 0.34 f19.97 ± 0.09 f132.63 ± 4.96 e6.23 ± 0.15 e18.29 ± 0.09 b
GF2+GF78.91 ± 0.14 ab6.13 ± 0.15 b0.51 ± 0.08 d31.87 ± 0.35 e20.31 ± 0.18 e134.98 ± 5.69 e6.98 ± 0.19 e17.99 ± 0.11 c
Source of
S**********
H--*********-
S×H--***********
Note: TS is soil total salt content, TN is soil total nitrogen content, AN is soil available nitrogen, AP is soil available phosphorus, AK is soil available potassium, SOM is soil organic carbon, and CEC is soil cation exchange capacity. Mean ± standard deviation. S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level, and ** indicates significance at 0.01 level; and - indicates irrelevant. Lowercase letters indicate significance at p < 0.05.
Table 4. Changes in soil salt and alkali ions after the application of degrading bacteria in soils with different salinity levels.
Table 4. Changes in soil salt and alkali ions after the application of degrading bacteria in soils with different salinity levels.
SalinityHandleCl−
(g/kg)		SO42−
(g/kg)		HCO3−
(g/kg)		CO32−
(g/kg)		Ca2+
(g/kg)		Mg2+
(g/kg)		Na+
(g/kg)		K+
(g/kg)
LCK1.15 ± 0.05 d2.15 ± 0.15 d0.41 ± 0.06 d0.15 ± 0.02 c0.51 ± 0.02 d0.36 ± 0.02 c1.09 ± 0.15 e0.15 ± 0.02 d
GF20.89 ± 0.15 e1.99 ± 0.09 e0.36 ± 0.05 d0.12 ± 0.02 c0.42 ± 0.03 d0.35 ± 0.03 c0.91 ± 0.26 f0.13 ± 0.01 d
GF70.88 ± 0.11 e1.89 ± 0.08 e0.37 ± 0.05 d0.13 ± 0.03 c0.35 ± 0.05 e0.32 ± 0.01 c0.86 ± 0.19 f0.12 ± 0.02 d
GF2+GF70.78 ± 0.12 e1.84 ± 0.12 e0.32 ± 0.03 d0.14 ± 0.04 c0.32 ± 0.04 e0.33 ± 0.02 c0.85 ± 0.12 f0.13 ± 0.02 d
MCK2.36 ± 0.06 c3.15 ± 0.15 c0.81 ± 0.09 c0.31 ± 0.02 b0.81 ± 0.03 c0.71 ± 0.03 b1.41 ± 0.26 c0.36 ± 0.01 c
GF21.12 ± 0.15 d2.59 ± 0.17 d0.71 ± 0.08 c0.29 ± 0.02 b0.79 ± 0.02 c0.69 ± 0.03 b1.22 ± 0.33 d0.33 ± 0.02 c
GF71.33 ± 0.08 d2.41 ± 0.21 d0.69 ± 0.04 c0.28 ± 0.03 b0.78 ± 0.03 c0.65 ± 0.05 b1.23 ± 0.15 d0.32 ± 0.05 c
GF2+GF71.32 ± 0.09 d 2.01 ± 0.06 de0.65 ± 0.06 c0.29 ± 0.01 b0.75 ± 0.01 c0.62 ± 0.04 b1.19 ± 0.26 d0.34 ± 0.02 c
HCK4.01 ± 0.08 a5.37 ± 0.14 a1.45 ± 0.05 a0.52 ± 0.02 a1.12 ± 0.02 a1.02 ± 0.02 a2.01 ± 0.36 a0.51 ± 0.02 a
GF22.81 ± 0.14 c4.15 ± 0.05 b0.98 ± 0.03 b0.45 ± 0.03 a0.93 ± 0.03 b0.93 ± 0.02 a1.87 ± 0.14 b0.45 ± 0.04 b
GF73.06 ± 0.15 b3.98 ± 0.09 b0.95 ± 0.08 b0.43 ± 0.03 a0.95 ± 0.02 b0.95 ± 0.03 a1.85 ± 0.18 b0.43 ± 0.06 b
GF2+GF72.98 ± 0.09 c 3.91 ± 0.11 bc0.91 ± 0.06 b0.43 ± 0.02 a0.96 ± 0.02 b0.91 ± 0.02 a1.77 ± 0.28 b0.41 ± 0.01 b
Source of
S**********
H**----*-
S×H***--*---
Note: Cl−, SO42−, CO32−, HCO3−, Ca2+, Mg2+, Na+, and K+ are saline–alkali ions in soil. S, H, and S×H denote the saline–alkali gradient, fertilization treatment, and the interaction effect between the two, respectively. * indicates significance at 0.05 level, and ** indicates significance at 0.01 level; and - indicates irrelevant. Lowercase letters indicate significance at p < 0.05.
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MDPI and ACS Style

Zhao, X.; Yu, X.; Gao, J.; Qu, J.; Borjigin, Q.; Meng, T.; Li, D. Improvement of Saline–Alkali Soil and Straw Degradation Efficiency in Cold and Arid Areas Using Klebsiella sp. and Pseudomonas sp. Agronomy 2024, 14, 2499. https://doi.org/10.3390/agronomy14112499

AMA Style

Zhao X, Yu X, Gao J, Qu J, Borjigin Q, Meng T, Li D. Improvement of Saline–Alkali Soil and Straw Degradation Efficiency in Cold and Arid Areas Using Klebsiella sp. and Pseudomonas sp. Agronomy. 2024; 14(11):2499. https://doi.org/10.3390/agronomy14112499

Chicago/Turabian Style

Zhao, Xiaoyu, Xiaofang Yu, Julin Gao, Jiawei Qu, Qinggeer Borjigin, Tiantian Meng, and Dongbo Li. 2024. "Improvement of Saline–Alkali Soil and Straw Degradation Efficiency in Cold and Arid Areas Using Klebsiella sp. and Pseudomonas sp." Agronomy 14, no. 11: 2499. https://doi.org/10.3390/agronomy14112499

APA Style

Zhao, X., Yu, X., Gao, J., Qu, J., Borjigin, Q., Meng, T., & Li, D. (2024). Improvement of Saline–Alkali Soil and Straw Degradation Efficiency in Cold and Arid Areas Using Klebsiella sp. and Pseudomonas sp. Agronomy, 14(11), 2499. https://doi.org/10.3390/agronomy14112499

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