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Article

Alfalfa Increases the Soil N Utilization Efficiency in Degraded Black Soil Farmland and Alleviates Nutrient Limitations in Soil Microbes

by
Linlin Mei
†,
Yulong Lin
†,
Ang Li
,
Lingdi Xu
,
Yuqi Cao
and
Guowen Cui
*
College of Animal Science and Technology, Northeast Agricultural University, Harbin 150000, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(10), 2185; https://doi.org/10.3390/agronomy14102185
Submission received: 2 August 2024 / Revised: 19 September 2024 / Accepted: 21 September 2024 / Published: 24 September 2024
(This article belongs to the Section Soil and Plant Nutrition)
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Versions Notes

Abstract

:
Alfalfa (Medicago sativa L.) can fix N naturally within soils, which makes alfalfa cultivation useful for enhancing soil fertility while minimizing environmental impacts from pesticides, fertilizers, and soil pollution. To assess the influence of alfalfa cropping on degraded black soil, we determined the nutrient stoichiometry of the soil and soil microbial biomass under four corn cultivation systems at the Harbin Corn Demonstration Base (Heilongjiang, China), which is located in Wujia (126°23′ E, 45°31′ N), Shuangcheng district, Harbin, Heilongjiang Province. The cultivation systems included continuous corn cultivation for more than 30 years (CK), 2 years of alfalfa–corn rotation (AC), three years of alfalfa cropping (TA), and four years of alfalfa cropping (FA). Overall, AC, TA, and FA treatment increased the soil pH, reduced the soil salinity, and increased the organic matter content of the 0–15 cm soil layer. TA and FA presented soil nutrient levels comparable to those of degraded cornfields that were fertilized annually. The TA and FA treatments increased the soil available N:P, soil N:P, and soil C:P ratios. Moreover, TA significantly increased the soil microbial biomass P (SMBP) in the 0–15 cm (surface) soil layer and reduced the soil microbial biomass C (SMBC):SMBP ratio. AC, TA, and FA increased the storage and mineralization rates of soil N and alleviated the microbial P limitations in degraded black soil farmland. Compared with FA, TA resulted in greater improvements in the quality of degraded black soil farmland. The ability of alfalfa to enhance soil fertility makes an important component of sustainable agricultural practices aimed at rehabilitating degraded soils.

1. Introduction

The black soil region in China, which is one of the world’s three major black soil zones, is primarily located in the northeastern region [1]. However, the quality of black soil on farmlands has been severely degraded, with decreases in the extent of the black soil area and fertility in recent years [2]. Moreover, the cultivation period of black soil farmland has continued to increase, and the contents of carbon (C), nitrogen (N), and various combined forms of humus in the soil have decreased accordingly [3]. Corn monoculture is a widely employed agricultural practice in China’s farming regions. However, this system poses several specific challenges, including a heightened risk of water and soil erosion, excessive consumption of water and fertilizer, and the deterioration of soil quality [4], which often results from soil nutrient depletion and compaction due to prolonged cultivation without proper crop rotation [5]. Thus, fertilizer application is key for enhancing crop productivity in this area. However, fertilizer use results in increased production costs and significant long-term environmental challenges [6]. Nonabsorbable fertilizers applied to plants tend to undergo losses through leaching [7], causing various nutrient imbalances and strongly affecting the sustainability of the environment and agricultural production [8]. Furthermore, the persistent high yields achieved through excessive fertilization have created a negative feedback loop of overexploitation of agricultural resources in cropped areas, ultimately leading to a deterioration in soil quality and a decline in the yield of agronomic crops [7]. These problems can be solved by modifying the agricultural system.
Rotations involving crops belonging to Poaceae and Leguminosae are considered efficient agricultural strategies for restoring degraded black soil [9,10,11]. The symbiotic N fixation performed by leguminous crops can result in increased crop yields and allow reductions in chemical fertilizer (e.g., N and P fertilizers) inputs, thereby ensuring food security and promoting sustainable agricultural development [12]. A previous study revealed that leguminous plants provide N to crop rotation systems and that root zone N deposition by leguminous crops is a key factor in determining the N resources available for subsequent crops [12]. Soybean (Glycine max L.) and corn (Zea mays L.) rotation increases crop yield and soil organic matter content [12]. The inclusion of leguminous crops in rotations can improve soil nutrient utilization efficiency and inhibit the harmful effects of pathogens on subsequent crops. Additionally, leguminous crops can alter soil conditions (e.g., soil moisture content, pH, and soil nutrient content) by promoting the proliferation of specific beneficial microbial communities [13,14]. Sustainable crop rotation methods have great potential for alleviating the degradation of the soil environment caused by continuous cropping [4,13]. The rotation of poaceae and leguminosae crops not only has enormous social value but also provides significant ecological benefits, including improving soil fertility, reducing the occurrence of pests and diseases, and inhibiting the growth of pathogens and pests [12].
The perennial leguminous forage crop alfalfa (Medicago sativa L.), which has high nutritional value and wide adaptability, is the main cultivated and processed forage crop in northern China [9,13]. Owing to the high crude protein content of alfalfa (between 16% and 22%), it can meet the dietary needs of ruminants and is a valuable resource for livestock nutrition [14]. Alfalfa can obtain soil phosphorus (P) from root exudates and arbuscular mycorrhizal fungi, thereby promoting symbiotic N fixation. As a crop that serves as a microbial hotspot, alfalfa has unique biological and economic advantages [13,15].
However, many uncertainties remain regarding the impact of alfalfa cultivation on the restoration of degraded black soil. Previous studies on the restoration of sandy grasslands have shown significant increases in soil organic C, total N, total P, and available P (AP) contents [16]. The impact of alfalfa on soil properties is influenced by various environmental factors (e.g., temperature and humidity) and water and fertilizer management measures. A study suggested that continuous cultivation of alfalfa for up to ten years may lead to a decrease in soil total N, total C, nitrate N, and available potassium (K) [17]. In addition, continuous cropping of alfalfa can accelerate the consumption of soil moisture and P resources [18,19].
Soil microorganisms are important driving factors of the complex transformation and cycling of soil organic matter and essential nutrients (including C, N, P, and sulphur (S)). They play a crucial role in decomposing organic matter and promoting the formation of humus, thus making significant contributions to soil fertility [20]. During the decomposition process, these microorganisms can fix inorganic nutrients in the soil and convert them into microbial biomass reserves of C, N, P, and S [21]. These reserves, in turn, become important sources of nutrients for plant growth [22]. However, the biomass and activity of soil microorganisms are limited by the availability of nutrients such as C, N, and P [22]. Early research indicated that soil microbes are C limited [23], whereas recent studies have emphasized the importance of N and P availability as key factors limiting microbial growth [24]. The patterns of N and P limitations observed for microbes are similar to those observed for plants [25]. In addition, the stoichiometric characteristics of C, N, and P in soil microorganisms can be used to predict potential changes in soil nutrient dynamics [26].
Our current understanding of these stoichiometric characteristics is insufficient. A deeper understanding of the complex relationships between soil microorganisms and their surrounding environment will enable us to better manage soil fertility and make sustainable improvements. The main purpose of this work was to study the impact of alfalfa cultivation on possible soil nutrient enhancement in degraded black soil farmland. We conducted a comparative analysis among multiple planting scenarios: long-term corn cultivation spanning over thirty years, a two-year rotation of alfalfa and corn, three consecutive years of alfalfa planting, and a four-year period of continuous alfalfa cultivation. The stability and interpretability of the results were improved through principal component analysis, and a deeper understanding of the potential changes in soil nutrient dynamics was obtained. It was anticipated that (1) cultivating alfalfa on degraded black soil farmland would enhance the efficiency of plant N utilization and that (2) incorporating alfalfa into crop rotation strategies could mitigate nutrient constraints.

2. Materials and Methods

2.1. Study Site

The study site was located in Wujia (126°23′ E, 45°31′ N) within the Shuangcheng district, Harbin, Heilongjiang Province. The area has a continental monsoon climate and a thin layer of black soil that is typical of agricultural areas. It is windy in spring and mostly rainy in summer. The autumn season is cool, and frost occurs early. The annual precipitation is 400–600 mm, and the precipitation is mainly concentrated in summer (June to August), during which time there is abundant rainfall. There is less precipitation in winter, mainly in the form of snowfall. The annual average temperature is 3.5–4.5 °C, the frost-free period is 142 days, and the effective growing season is 142 days. The average temperature in winter (December to February of the following year) is usually between −10 °C and −20 °C, with extremely low temperatures reaching −30 °C. The average temperature in summer (June to August) is approximately 20 °C. According to the world reference base for soil resources (WRB) 4th edition, 2022, the soil types are phaeozems and chernozems [26]. The granulometric composition of the genetic horizons at a depth of 1.5 m is 30% gravel, 40% silt, and 20% clay. The soil pH was 5.9.

2.2. Experimental Design

Land with degraded black soil that has been continuously cropped with corn for more than 30 years was the focus of this study. The experiment involved a completely randomized block factorial layout and involved four distinct treatment conditions: continuous corn cultivation for more than 30 years (CK), corn cultivation in 2019 after 2 years of alfalfa cropping in 2017 and 2018 (AC), 3 years of alfalfa (TA) cropping, and 4 years of alfalfa (FA) cropping. Each treatment was replicated four times. The plot size was 20 m × 20 m, and each plot was set 5 m apart. The plots exhibited a level terrain, with a consistent homogeneous soil composition. Our research was conducted from 2016 to 2019.
The corn and alfalfa cultivars were “Tiannong 9” and “Dongnong 1”, respectively. Tiannong 9 is a widely cultivated variety in the local area. Dongnong 1 is salt-,alkali- and cold-resistant. In the local planting systems, a total of 600 kg·hm−2 compound fertilizer consisting of 72 kg·hm−2 N, 108 kg·hm−2 P, and 90 kg·hm−2 K was added to the corn field every year. Alfalfa was sown in May 2016 in the FA treatment and May 2017 in the TA treatment. In the years when alfalfa was sown, the alfalfa fields were fertilized with 54 kg·hm−2 N and 138 kg·hm−2 P. A foliar spray (2% urea) was applied 10 days prior to each alfalfa harvest by mowing.

2.3. Soil and Sampling

In mid-September 2019, soil samples were collected following crop harvest. Within each designated plot, ten random sample points were chosen, and the soil was sampled using a soil auger with a diameter of 2.5 cm. The soils collected from these points were thoroughly mixed to form a composite sample. The taproots of alfalfa are deep and can reach more than 30 cm into the soil. Therefore, samples were collected from two soil depths: 0–15 cm (surface soil) and 15–30 cm (subsurface soil). After plant litter was removed from the soil surface, the soil samples were air-dried; subsequently, to ensure the particles had a homogeneous particle size for accurate assessment of the soil parameters, the samples were sieved through a 2 mm mesh.

2.4. Laboratory Analyses

The bulk density (BD) of the soil was measured using a standardized ring knife method, which allows the calculation of the soil mass per unit volume [27]. The moisture content (MC) of each soil sample was determined by a gravimetric approach; the soil samples were dried at a constant temperature of 105 °C until a consistent weight was achieved, indicating the complete elimination of moisture, and the difference in weight before and after drying was taken as the water content. The soil electrical conductivity (EC) was measured using a conductivity meter. The soil pH was tested using a pH meter [28]. Soil organic matter (SOM) content was determined using the K dichromate oxidation oil bath heating method [29].
The soil ammonium N (NH4+-N) and nitrate N (NO3−-N) contents were measured using a continuous flow analyzer (Futura II, Alliance Instruments Ltd., Paris, France), and the soil available N (AN) content was calculated as NH4+-N+NO3−-N. The soil AP was extracted with 0.5 mol/L sodium bicarbonate (NaHCO3) and analyzed by using the molybdate blue colorimetric method at a wavelength of 880 nm [24]. The soil organic C and total N contents were measured individually by employing a stable isotope mass spectrometer (Isoprime 100, Isoprime Ltd., Manchester, UK) [30]. Total P was measured using the molybdenum blue ascorbic acid method after sulfuric acid hydrogen peroxide (H2SO4-H2O2) digestion [31]. After chloroform fumigation extraction, the soil microbial biomass C (SMBC) and soil microbial biomass N (SMBN) were quantified on the basis of the dry weight of the soil. Extraction was carried out using a ratio of 20 g of soil to 80 mL of a 0.5 M K2SO4 solution (1:4) [31]. The obtained solution was subsequently analyzed to assess the C and N contents of the soil microbial biomass by utilizing a TOC-L CPH analyzer (manufactured by Japan Shimadzu as a total organic C analyzer). After extraction using a solution of 0.5 mol/L NaHCO3, we conducted a comprehensive survey of soil microbial biomass P (SMBP) by employing the molybdate blue colorimetric method. Finally, the values of SMBC, SMBN, and SMBP were successfully determined [22,25].

2.5. Statistical Analysis

The Shapiro-Wilk test yielded the following statistical results: W = 0.923 and p = 0.057. The data in this study followed a normal distribution. The data were subjected to the Kaiser-Meyer-Olkin (KMO) and Bartlett tests (Supplementary Tables S1 and S2) [32,33]. By utilizing one-way ANOVA and principal component analysis (PCA), we assessed the stoichiometric ratios of the soil and microbial biomass. All the data analyses and graphical representations were executed in SPSS 26 and Origin 2019b, respectively. Tukey’s test was employed to compare means and ensure accuracy and reliability in the statistical evaluation (p < 0.05).

3. Results

3.1. Soil Parameters

To determine the effects of alfalfa cultivation on soil fertility parameters, we first aimed to determine the physicochemical properties of the soil in each treatment by analyzing the soil samples. The physicochemical characteristics of the soil samples showed notable variations in response to distinct planting techniques. Compared with the control group, both the TA and FA treatments markedly decreased the MC by 7.12% and 8.58% (p < 0.05) within the surface soil layer, respectively, while simultaneously increasing the soil BD by 27.59% and 32.08% (p < 0.05), respectively. On the other hand, compared with the control group, the AC, TA, and FA treatments significantly elevated the pH by 6.92%, 6.59% and 6.08% (p < 0.05) and concurrently lowered the soil electrical conductivity by 44.21%, 57.18% and 60.67% (p < 0.05) within the surface soil layer, respectively. Furthermore, FA decreased the soil SOM by 19.14% (p < 0.05) within the subsurface layer (Table 1).

3.2. Soil AN and AP and Corresponding Ratios

Compared with those in the control group, the AC and FA treatments decreased the soil NH4+-N content by 42.16% and 41.54%, respectively, in the surface soil and by 62.74% and 35.23%, respectively, in the subsurface soil (p < 0.05, Figure 1A); the AC treatment increased the soil NO3−-N content by 15 times, reaching 1584.88% (p < 0.05) in the surface soil; and the AC and TA treatments increased the soil NO3−-N content by 28 times and 40 times, respectively, by 2834.17% and 3954.68%, in the subsurface soil (p < 0.05, Figure 1B).
AC, TA, and FA had no influence on the AN in the surface soil. However, TA and FA decreased the AN by 12.03% and 31.20%, respectively (p < 0.05, Figure 2A), in the subsurface soil. AC, TA, and FA decreased the AP by 60.86%, 60.91%, and 65.83% (p < 0.05, Figure 2B) in the surface soil, respectively, but had no influence on the AP in the subsurface soil (Figure 2B).
AC, TA, and FA increased the soil AN:AP ratio by 184.52%, 136.71%, and 135.12% (p < 0.05, Figure 2C) in the surface soil; however, it had no influence on the soil AN:AP ratio in the subsurface soil (Figure 2C).

3.3. Soil Nutrients and Stoichiometric Ratios

AC, TA, and FA had no influence on soil organic C or total N but reduced the total P by 29.43%, 40.38%, and 43.02% (p < 0.05, Figure 3A–C) in the surface soil, respectively; FA reduced the organic C and total P by 19.07% and 28.90% (p < 0.05, Figure 3A–C) in the subsurface soil, respectively. These data indicate that alfalfa cultivation generally resulted in a decrease in the soil P content in both soil layers.
AC, TA, and FA had no influence on the C:N ratio in the surface soil; however, TA and FA decreased the C:N ratio in the subsurface soil by 15.80% and 13.29%, respectively (p < 0.05, Figure 3D). TA and FA increased the N:P ratio by 78.78% and 67.32%, respectively, in the surface soil and by 21.78% and 30.40%, respectively, in the subsurface soil (p < 0.05, Figure 3E). TA and FA increased the C:P ratio by 72.50% and 64.31% (p < 0.05, Figure 3F), respectively, in the surface soil; the planting method had no influence on the C:P ratio in the subsurface soil (Figure 3F).

3.4. Soil Microbial Biomass Stoichiometry

FA decreased SMBC by 52.59% (p < 0.05) in the surface soil, and AC, TA, and FA had no influence on SMBC in the subsurface soil (Figure 4A). TA and FA increased SMBN by 107.04% and 205.63% (p < 0.05) in the surface soil, respectively; FA increased SMBN by 341.38% (p < 0.05, Figure 4B) in the subsurface soil. AC, TA, and FA decreased SMBP by 5.64%, 85.63%, and 47.19%, respectively (p < 0.05, Figure 4C), in the subsurface soil.
TA and FA decreased the SMBC:SMBN ratio by 66.07% and 88.08%, respectively, in the surface soil; FA decreased the SMBC:SMBN ratio by 85.12% (p < 0.05, Figure 4D) in the subsurface soil. FA increased the SMBN:SMBP ratio by 131.40% (p < 0.05, Figure 4E) in the surface soil. TA and FA decreased the SMBC:SMBP ratio by 56.66% and 59.04% (p < 0.05, Figure 4F) in the surface soil, respectively; AC, TA, and FA had no influence on the SMBN:SMBP and SMBC:SMBP ratios in the subsurface soil (Figure 4E,F). The correlation between soil surface and subsurface moisture content (MC%), bulk density (BD), pH value, electrical conductivity (EC), and soil stoichiometry characteristics with SMBC, SMBN, and SMBP under different planting methods are shown in Supplementary Tables S3 and S4.

3.5. Principal Component Analysis

To further investigate the relationships between planting methods and soil and soil microbial biomass, principal component analysis (PCA) was performed. The variance contribution rate of the first principal component (PCA1) was 54.7%, and the variance contribution rate of the second principal component (PCA2) was 24.4%; together, these axes explained a total of 79.1% of the variance in the variables. AC, TA, and FA had different effects on the stoichiometry of the soil and soil microbial biomass in the surface soil layer. The continuously cropped corn field was separated from the three-year and four-year alfalfa fields, and AC, TA, and FA had similar distributions. CK was located on the negative side of the axis of PCA1, whereas TA was located on the negative side of the axis of PCA2. Figure 5A shows that CK had a significant effect on the SMBC:SMBP and SMBC:SMBN ratios, TA had a significant effect on the soil N:P ratio, and FA had a significant effect on the SMBN:SMBP ratio. The soil C:N ratio was less affected by FA, whereas the soil C:P ratio was less affected by CK (Figure 5A).
In the subsurface soil, the variance contribution rate of PCA1 was 39.8%, and the variance contribution rate of PCA2 was 26.0%; together, these axes explained 65.8% of the variance. The planting methods had different impacts, and CK and AC were separated from TA and FA. CK was located on the negative side of the axis of PCA1, whereas FA was located on the positive side of the axis of PCA1. CK had a significant effect on the soil C:N and SMBC:SMBN ratios, TA had a significant effect on the SMBN:SMBP and SMBC:SMBP ratios, and FA had a significant effect on the soil C:P and N:P ratios.

4. Discussion

Remarkable soil improvements were observed in the alfalfa rotation practices, as reflected by increased pH levels, reduced soil salinity, and consistent surface soil SOM contents. Even in the absence of fertilization, alfalfa fields presented soil nutrient levels comparable to those of annually fertilized but degraded cornfields. The TA and FA treatments increased the soil AN:AP, N:P, and C:P ratios. Moreover, TA significantly increased the SMBP content in the surface soil layer and reduced the SMBC:SMBP ratio. Alfalfa cultivation significantly increased soil N storage and associated mineralization processes, thereby mitigating microbial P constraints in rehabilitated black soil croplands. Compared with FA, TA had a greater effect on restoring the fertility of degraded black soil farmland.
The long-term fertilization of farmland leads to soil salinization, affecting soil nutrient cycling, causing significant negative impacts on crop growth and yield [34] and posing a threat to global agricultural production and food security. Moreover, changes in soil parameters affect plant growth and soil microbial communities [24]. In the present study, planting alfalfa had no significant effect on the SOM content of the 0–15 cm soil layer, but the SOM content of the FA soil was significantly lower than those of the CK and AC soils. On the one hand, due to the effect of increasing SOM after alfalfa planting, it requires a certain amount of time for accumulation [35]. On the other hand, it may be related to the distinct planting and management modes employed for corn and alfalfa. In the local planting systems, a total of 600 kg·hm−2 compound fertilizer consisting of 72 kg·hm−2 N, 108 kg·hm−2 P, and 90 kg·hm−2 K was added to the corn field every year. In the process of fertilizing corn fields, using deep soil fertilization can reduce nutrient volatilization and loss, improve fertilizer utilization efficiency, and thus contribute to the accumulation of soil organic matter [36,37]. Meanwhile, the corn roots remain embedded in the soil even after harvesting. In contrast, during annual alfalfa harvest, which occurs three times a year in TA and FA treatment, an overwhelming majority of the aboveground biomass is removed. Consequently, only a minimal quantity of litter might penetrate the soil during alfalfa cultivation, and SOM might remain within the surface stratum [17]. Nevertheless, no organic materials were added to the subsurface layer; furthermore, alfalfa requires a considerable amount of nutrients to grow, which leads to a decrease in the SOM in this particular layer [33]. Research has demonstrated that planting alfalfa on degraded cultivated land can significantly increase the soil SOM content [38,39]. These findings indicate that under various management practices, alfalfa cultivation sustains the surface soil SOM content, and the surface soil SOM content in alfalfa fields remains consistent with that in corn fields, suggesting that alfalfa cropping positively influences the soil SOM content.
Soil N mineralization is an important component of soil N cycling, and the rate of N mineralization depends on the organic N quantity, temperature, MC, and microbial activity rates [40,41]. Numerous studies have shown that planting alfalfa can increase the total N content in the soil [34,42]. In the surface soil layer in this study, AC and FA reduced the soil NH4+-N content but had no significant effect on the soil AN content. This occurred because although alfalfa can fix N, it also consumes a large amount of N. The changes in the soil total N after alfalfa cropping were consistent with those in the soil SOM, and there was no significant difference in the total N content compared with that in the CK. The total N content of AC was significantly greater than that of FA only in the subsurface soil layer. A study has shown that organic N accounts for more than 95% of the total N content in black soil and that there is a highly significant positive correlation between organic C and total N in black soil areas [43]. The intensity of soil N accumulation in artificial grasslands mainly depends on the inputs of plant roots and aboveground organic residues into the soil, as well as factors such as the decomposition and transformation of input materials in the soil [21].
In the present study, alfalfa was cut three times a year, and very little organic residue entered the soil from the aboveground parts. Changes in the N content of the soil occurred mainly because of root nodule-driven N fixation by alfalfa [44]. Studies have shown that for every 1000 kg of alfalfa hay harvested, 32 kg of N is removed from the soil [35,38]. Planting alfalfa can provide 40% to 60% of the required N [14]. Nonetheless, in the present study, although fertilizer was not applied to the alfalfa fields after the first year of cropping, the total N content of the alfalfa cropping soil was not significantly different from that of the continuously fertilized corn field. Moreover, the total N content of TA was slightly greater than that of CK, indicating that the N-fixing effect of alfalfa was significant. This finding closely aligns with findings from a previous study in which 10-year alfalfa fields and 10-year corn–wheat rotation fields accumulated essentially the same stocks of organic C, total N, and total P [42].
Soil organic C and soil N are important components of soil, and their relationship, i.e., the soil C:N ratio, plays a crucial role in determining soil fertility and ecosystem stability [45]. Additionally, the soil C:N ratio is an indicator of the soil N mineralization capacity and is closely related to fertilization practices, microbial distribution, etc. [30]. Moreover, the soil C:N ratio is inversely proportional to the rate of SOM decomposition. When the C:N ratio is high, microbes need N inputs to meet their growth needs; when the C:N ratio is low, N exceeding that required for microbial growth is released into the soil [46]. During the second soil survey in China, the C:N ratio showed little variation among different climatic zones, soil grades, soil depths, and weathering stages [47]. In the present study, the C:N ratio (10.06–14.76) was slightly greater than the average C:N ratio of Chinese soils (10–12). This means that soil N is relatively insufficient and may also have certain impacts on microbial activity and soil environment [45]. The total N content of AC in the subsurface soil layer was significantly greater than that of FA, which is consistent with previous research findings [48] and was slightly greater than that of CK. TA and FA significantly reduced the soil C:N ratio. Alfalfa has a high efficiency in absorbing and utilizing N during its growth process, which may accelerate the turnover of N in the soil, relatively increase the N content, and reduce the C:N ratio [42]. Meanwhile, the growth of alfalfa may stimulate the activity of soil microorganisms. Microorganisms preferentially utilize N when decomposing organic matter, resulting in an increase in relative N content and decrease in soil C:N ratio [14]. These findings indicate that planting alfalfa on degraded farmland with long-term corn cultivation can effectively improve soil N utilization efficiency and improve soil quality.
P is an essential element for plant growth and development, and it has a significant effect on the morphology and physiology (e.g., root growth, nutritional growth, and hormone regulation) of plants [31]. In agricultural environments, the natural P fertility of soils is altered by nutrient uptake by crops and nutrient inputs from fertilization [49,50]. The P present in soil undergoes adsorption and fixation by minerals; as a result, more than 95% of the soil P content is unusable and unavailable for plant growth [51]. Consequently, the rate at which plants can utilize P from the soil is typically quite low. In terms of TA and FA, the total P and AP contents in the soil were significantly lower than those after long-term corn cultivation, and the P content in FA was slightly lower than that in TA. Alfalfa requires a high amount of P. The longer the cropping period is, the greater the consumption of P in the soil [18,34]. To achieve high yields and yield increases, a large amount of N, P, and K compound fertilizer must be applied to corn fields every year. The AP in the surface soil layer of corn fields can reach 89.36 mg·kg−1, far exceeding the environmental threshold of 50.0 mg·kg−1 in China’s soil environmental quality standards [48]. However, in alfalfa fields, no soil fertilizer was applied after base fertilizer application in the first year of planting, and only AP could be consumed each year from the soil. Additionally, the formation of insoluble P in the soil could lead to a decrease in total P levels due to the conversion of P into unavailable forms (e.g., P combined with other elements and P in deep soil) [52]. In addition, the AP content in AC was 35.0 mg·kg−1, which was between the values for the agronomic threshold of AP in black soils (15.5 mg·kg−1) and the environmental threshold for significant leaching (50.0 mg·kg−1) [53]. These findings indicate that the soil AP content after alfalfa planting could meet the needs for subsequent crop growth without causing water pollution and had a positive effect on the soil nutrient balance.
The soil C:N:P ratio regulates not only microbial activity but also the uptake of nutrients such as N and P by plants [30]. It integrates the effects of variability in ecosystem functions and is the main indicator reflecting C, N, and P cycling within soils [23]. A previous study revealed that the soil N:P ratio is greater in the third year of alfalfa cultivation than in other years, and the soil N:P ratio varies within the same planting year according to the duration of alfalfa cultivation [54]. In the present study, after TA and FA, the soil C:P ratio was significantly greater than that of the CK, and the soil C:P ratio ranged from 1.85 to 4.42, which was lower than the average soil C:P ratio in China (5.9) [55]. The N:P ratio can be used as a diagnostic indicator of N saturation and is used to determine the threshold for nutrient limitation [31]. The soil N:P ratios of TA and FA were significantly greater than those of CK. Fertilization leads to soil acidification, affects soil phosphatase activity, and weakens soil N and P coupling [21,56]. There was no fertilizer input to the alfalfa fields, and N was increasingly consumed due to alfalfa N fixation and a lack of P sources. The increase in N due to fixation by leguminous crops can potentially limit crop growth due to P limitations [57]. Under P limitation, leguminous plants respond by activating different P uptake strategies [58]. These strategies include enhancing soil P acquisition through root exudates or through binding with arbuscular mycorrhizal fungi [59], enhancing nodulation and N fixation processes, overcoming P shortages and optimizing crop growth [60]. This adaptability reflects the ability of leguminous crops to adapt to environmental nutritional limitations. Alfalfa roots maintain soil fertility by increasing the SOM content and promoting nodule-based N fixation. In the present study, AC, TA, and FA had no significant effects on the SMBC in the subsoil. The positive effects of alfalfa cultivation on soil microorganisms and fertility may be more pronounced in other soil layers or under different environmental conditions.
Soil microorganisms play a crucial role in soil material cycling [61]. Researchers have shown that alfalfa rotation with other crops can increase crop root growth and physiological activity, promote soil microbial activity, improve soil fertility, sustain the soil ecosystem balance, and improve plant productivity [21,62].
Soil microbial biomass and its changes are important indicators for evaluating soil fertility. Soil microorganisms are often limited by soil resources such as C, N, and P [63]. SMBN and SMBP are comprehensive indicators of soil microbial N and P mineralization and fixation and are important reservoirs of soil N and P. They can regulate the transformation processes of N and P [64,65]. A previous study revealed that the rotation of corn and soybean resulted in an increase in microbial biomass N of 85%–174% [12]. In the present study, the TA and FA treatments significantly increased the SMBN in the surface soil layer. These findings indicate that alfalfa rotation with other crops can increase soil N storage and mineralization rates by increasing soil microbial activity, which plays a crucial role in improving N availability [17]. Moreover, the rhizosphere microorganisms of alfalfa are protected during the corn growth cycle, ensuring their continued existence [13]. Leguminous crop cultivation can leave beneficial microorganisms in the soil and enrich N cycling-related genes in the rhizosphere microorganisms of subsequent crops [66].
Nutrient limitation in soil microorganisms is controlled by various factors, such as temperature; atmospheric N deposition; and changes in soil properties, such as the soil MC, soil nutrient status and pH [67,68]. Fertilization leads to severe soil salinization and a high calcium (Ca) ion content in the soil, and Ca easily combines with P in the soil to generate insoluble calcium phosphate compounds [2]. The SMBC:SMBP ratio is an important indicator for measuring the effectiveness of soil microbial P content, and a decrease in the SMBC:SMBP ratio indicates a decrease in microbial P limitation. In the present study, TA significantly increased SMBP in the surface soil layer. In the subsurface soil layer, the AC, TA, and FA treatments significantly reduced SMBP. This may be due to the vigorous growth of alfalfa in the surface soil, which has a relatively low degree of competition with microorganisms for nutrients such as P [16]. In deep soil, due to fewer root systems, it is more difficult for microorganisms to obtain P, and they may compete more fiercely with plant roots for P, leading to a decrease in microbial P production [69]. Furthermore, FA significantly increased the SMBN:SMBP ratio in the subsurface soil layer, and TA and FA significantly reduced the SMBC:SMBP ratio in the surface soil layer. Our results indicate that alfalfa cultivation effectively alleviates the limitations of soil microbial P in degraded black soil farmland. The decrease in the SMBC:SMBP ratio also indicates that planting alfalfa has great potential for promoting the release of P during soil microbial mineralization and transformation.

5. Conclusions

During long-term crop cultivation, the use of large amounts of chemical fertilizers is needed to maintain high yields, which can lead to high residual inorganic salt ions, exacerbate soil degradation, and inhibit soil element cycling. Our results demonstrated that alfalfa cropping not only helps to neutralize the pH of acidic soils but also reduces soil salinity in degraded black soil farmland and promotes the maintenance of the surface SOM content of the soil. Continuous cropping of alfalfa can reduce the need for chemical fertilizer inputs, and the soil nutrient content of alfalfa fields cultivated without fertilization is equivalent to that of degraded corn farmlands that are fertilized annually. Planting alfalfa on degraded black soil farmland can increase the soil N storage and mineralization rates and significantly increase N availability by increasing soil microbial activity. Moreover, the TA treatment significantly increased the SMBP in the surface soil layer and reduced the SMBC:SMBP ratio, indicating that alfalfa cropping effectively alleviated microbial P limitations in degraded black soil farmland. Compared with FA, TA had a greater effect on degraded black soil farmland in alleviating soil microbial P limitation. Soil microorganisms are indispensable for protecting biodiversity and promoting ecosystem functions, playing a key role in maintaining the Earth’s life support system and sustainable development. Alfalfa grown in rotation can recruit beneficial microbial groups that can improve soil nutrient utilization efficiency and inhibit the harmful effects of pathogens on subsequent crops. Alfalfa cultivation is a good strategy for enhancing subterranean microbial health and related functions, particularly in nutrient-deficient soils. Future studies should focus on harnessing the full potential of soil microorganisms by exploring the functional traits of microbes via metaproteomic or metatranscriptomic approaches.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14102185/s1, Table S1. KMO and Bartlett tests in the surface soil layer. Table S2. KMO and Bartlett tests in the subsurface soil layer. Table S3. The correlation between soil surface moisture content (MC%), bulk density (BD), pH value, electrical conductivity (EC), and soil stoichiometry characteristics with SMBC, SMBN, SMBP under different planting methods. Table S4. The correlation between soil subsurface moisture content (MC%), bulk density (BD), pH value, electrical conductivity (EC), and soil stoichiometry characteristics with SMBC, SMBN, SMBP under different planting methods.

Author Contributions

Validation, Y.L. and G.C.; Formal analysis, A.L.; Resources, L.X. and Y.C.; Writing—review & editing, L.M. 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 (32201469), the China Postdoctoral Science Foundation (2021M690575) and the Heilongjiang Provincial Natural Science Foundation Project (LH2022C034).

Data Availability Statement

Data is contained within the article and supplementary materials.

Acknowledgments

We would like to thank the anonymous reviewers for helpful comments on the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Effects of different planting practices on the NH4+-N (A) and NO3−-N (B) contents. The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm soil layers. The data are presented as the means ± standard errors (four repetitions).
Figure 1. Effects of different planting practices on the NH4+-N (A) and NO3−-N (B) contents. The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm soil layers. The data are presented as the means ± standard errors (four repetitions).
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Figure 2. Effects of different planting practices on the soil AN (A) and AP (B) contents and the AN and P ratios (C). The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm soil layers. The data are presented as the means ± standard errors (four repetitions).
Figure 2. Effects of different planting practices on the soil AN (A) and AP (B) contents and the AN and P ratios (C). The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm soil layers. The data are presented as the means ± standard errors (four repetitions).
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Figure 3. Soil organic C, total N, and total P contents (A–C) and stoichiometric ratios (D–F) under different planting practices. The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm soil layers. The data are presented as the means ± standard errors (four repetitions).
Figure 3. Soil organic C, total N, and total P contents (A–C) and stoichiometric ratios (D–F) under different planting practices. The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm soil layers. The data are presented as the means ± standard errors (four repetitions).
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Figure 4. Effects of different planting practices on the soil microbial biomass C, N, and P contents (A–C) and their stoichiometric ratios (D–F). The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm layers. The data are presented as the means ± standard errors (four repetitions).
Figure 4. Effects of different planting practices on the soil microbial biomass C, N, and P contents (A–C) and their stoichiometric ratios (D–F). The different lowercase and capital letters above the bars indicate significant differences (p < 0.05) among the different planting practices in the 0–15 cm soil layer and the 15–30 cm soil layer. The asterisks indicate significant differences (p < 0.05) between the 0–15 cm and 15–30 cm layers. The data are presented as the means ± standard errors (four repetitions).
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Figure 5. Effects of different planting practices on soil C:N:P stoichiometry (A) and soil microbial biomass stoichiometry (B).
Figure 5. Effects of different planting practices on soil C:N:P stoichiometry (A) and soil microbial biomass stoichiometry (B).
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Table 1. The impact of planting practices on soil physicochemical properties.
Table 1. The impact of planting practices on soil physicochemical properties.
0–15 cm Soil Layer15–30 cm Soil Layer
CKACTAFACKACTAFA
MC %26.74 ± 0.40 a26.32 ± 0.40 a24.84 ± 0.65 bc24.44 ± 0.22 b26.07 ± 0.29 a26.00 ± 0.77 a25.35 ± 0.54 a24.72 ± 0.13 a
BD g cm−31.06 ± 0.03 b1.12 ± 0.06 b1.35 ± 0.05 a1.40 ± 0.02 a1.20 ± 0.02 b1.04 ± 0.04 c1.31 ± 0.02 ab1.39 ± 0.05 a
pH5.92 ± 0.06 b6.33 ± 0.06 a6.31 ± 0.01 a6.28 ± 0.01 a6.63 ± 0.13 a6.88 ± 0.05 a6.76 ± 0.02 a7.00 ± 0.15 a
EC μs cm−181.70 ± 15.52 a45.58 ± 6.98 b34.98 ± 1.65 b32.13 ± 0.65 b48.45 ± 7.69 a48.75 ± 5.97 a35.23 ± 1.40 a47.43 ± 11.87 a
SOM g kg−128.79 ± 2.92 a27.83 ± 2.48 a28.32 ± 1.00 a27.02 ± 1.31 a27.46 ± 0.79 a28.47 ± 1.25 a24.30 ± 1.16 ab22.22 ± 1.39 b
The means ± standard errors are shown in the table (four repetitions). Different letters indicate significant differences (Tukey’s test, p < 0.05). Continuous corn cultivation for more than 30 years (CK); corn cultivation in 2019 after 2 years of alfalfa cropping in 2017 and 2018 (AC); 3 years of alfalfa (TA) cropping; and 4 years of alfalfa (FA) cropping.
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MDPI and ACS Style

Mei, L.; Lin, Y.; Li, A.; Xu, L.; Cao, Y.; Cui, G. Alfalfa Increases the Soil N Utilization Efficiency in Degraded Black Soil Farmland and Alleviates Nutrient Limitations in Soil Microbes. Agronomy 2024, 14, 2185. https://doi.org/10.3390/agronomy14102185

AMA Style

Mei L, Lin Y, Li A, Xu L, Cao Y, Cui G. Alfalfa Increases the Soil N Utilization Efficiency in Degraded Black Soil Farmland and Alleviates Nutrient Limitations in Soil Microbes. Agronomy. 2024; 14(10):2185. https://doi.org/10.3390/agronomy14102185

Chicago/Turabian Style

Mei, Linlin, Yulong Lin, Ang Li, Lingdi Xu, Yuqi Cao, and Guowen Cui. 2024. "Alfalfa Increases the Soil N Utilization Efficiency in Degraded Black Soil Farmland and Alleviates Nutrient Limitations in Soil Microbes" Agronomy 14, no. 10: 2185. https://doi.org/10.3390/agronomy14102185

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