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Article

Analyses of Rhizosphere Soil Physicochemical Properties and Microbial Community Structure in Cerasus humilis Orchards with Different Planting Years

by
Xiaopeng Mu
*,†,
Jing Wang
†,
Hao Qin
,
Jingqian Ding
,
Xiaoyan Mou
,
Shan Liu
,
Li Wang
,
Shuai Zhang
,
Jiancheng Zhang
and
Pengfei Wang
College of Horticulture, Shanxi Agricultural University, Jinzhong 030801, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Horticulturae 2024, 10(10), 1102; https://doi.org/10.3390/horticulturae10101102
Submission received: 14 August 2024 / Revised: 15 October 2024 / Accepted: 15 October 2024 / Published: 17 October 2024
(This article belongs to the Section Plant Nutrition)
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Abstract

:
Cerasus humilis has been widely used as a key ecological improvement plant species in barren lands in Northern China; however, the soil improvement effects of long-term C. humilis planting have rarely been reported. Our study aimed to determine the effects of planting C. humilis after 3, 6, and 10 years on the physicochemical properties and microbial community structures of the rhizosphere soil. pH decreased significantly with increasing time. Organic matter (OM), total phosphorus (TP), available phosphorus (AP), total potassium (TK), and available potassium (AK) increased gradually from 3 to 10 years. Alkaline and total nitrogen increased significantly and peaked at 6 years. Alkaline phosphatase, urease, sucrase, and hydrogen peroxide activities peaked at 6 years and decreased. Significant differences occurred in C. humilis rhizosphere bacterial and fungal community diversity and richness. Ace, Chaol, Shannon, and Simpson indices indicated diversity and richness of bacterial and fungal communities peaked at 3 and 10 years, respectively. Soil physicochemical properties, except pH, were positively significantly correlated with microbial community structure. AK and TK were the main factors for bacteria and fungi, respectively, with time. Increases in C. humilis rhizosphere soil microbial community relative abundance may be attributed to beneficial bacteria (Acidobacteria, Proteobacteria, and Actinobacteria) and fungi (Ascomycota, Mortierellomycota, and Basidiomycota). Physicochemical and soil and microbial community structure properties gradually improved; however, with time, adequate nutritional supplementation was needed to prevent decreased microbial community richness and diversity.

1. Introduction

Chinese dwarf cherry (Cerasus humilis (Bge.) Sok.), a perennial shrub in the Rosaceae family, not only has strong cold and drought resistance but also good adaptability to soils with moderate salinity and alkalinity [1,2]. Therefore, it has been widely used as a key plant species in soil improvement and water conservation projects [3]. Planting C. humilis in the Loess Plateau regions of Northern China significantly improves soil qualities and reduces soil erosion [4,5]. Other studies revealed that using C. humilis for vegetation restoration in coal mine areas can significantly increase the total nitrogen (TN), total phosphorus (TP), total potassium (TK), and organic matter (OM) content of the reclaimed land [6,7].
The rhizosphere is a hotspot where materials are actively exchanged between roots and soil [8]. In addition, the root surface and rhizosphere soil contain important microbial communities that play indispensable roles in improving root health and plant growth [9,10,11,12]. Recently, studies have shown that plant root exudates could selectively recruit protective microorganisms and enhance their microbial activity [10]. Plants have unique and representative rhizosphere microbial communities because of their different root exudates, which could shape the networks of rhizosphere microorganisms by providing necessary nutrients and boosting microbial carbon metabolism [13,14]. It has been reported that Bacteroidetes, Proteobacteria, and other eutrophic organisms have been enriched in the rhizosphere and these microorganisms could benefit plants by inhibiting pathogen invasion and activating soil nutrients [15].
Plant age and physiological state have also been reported to affect rhizosphere microbial composition [16]. For example, pecan age significantly influenced bacterial and fungal community structure in rhizosphere soil, which was driven by changes in pH value and AP content [17]. Some researchers have studied the effects of planting C. humilis on soil fertility and the rhizosphere microbial community [9,18]. However, the interrelationships between rhizosphere soil physicochemical indicators, enzyme activity, and microbial communities in different planting years remain unclear.
In this study, we evaluated 3-, 6-, and 10-year-old rhizosphere soil after planting C. humilis orchards by analyzing their physicochemical properties and soil enzyme activities. Moreover, changing in the structure of soil bacteria and fungi were determined through high-throughput sequencing technology. Results of this study will be of great importance for the scientific evaluation of the value of C. humilis as an ecological improvement tree species and for understanding its rhizosphere microbial ecology, soil improvement effects, and planting management.

2. Materials and Methods

2.1. Description of the Study Area

The experimental site was located in the Juxin Experimental Orchard (112.55° E, 37.42° N) in Jinzhong, China (Figure 1). This location is characterized a typical temperate continental climate, with an altitude of 767–900 m. The annual average temperature, rainfall and frost-free period are 9.9 °C, 400–500 mm, and 175–180 d, respectively. The soil of this area has the following properties: pH of 8.47, organic matter contents of 10.96 mg·kg−1 available N, P and K level of 58.03, 9.70, and 79.08 mg·kg−1, respectively.

2.2. Experimental Design

The C. humilis variety 99-02 provided by Shanxi Agricultural University was used as the experimental material. One-year-old C. humilis seedlings were planted in the experimental areas in spring of 2013, 2017, and 2020, respectively. During the growth of C. humilis, measures such as weeding and pest and disease prevention were taken, and no irrigation or fertilizer was applied.
Soil samples collection was conducted on 5 April 2023. Each sample was a blend of rhizosphere soil from ten random C. humilis plants with the same planting year. Bulk soils from five random spots (at least 1 m away from the planting row) were mixed and used as the control (Figure S1). During sampling, we firstly removed the surface litter and larger stones, and then excavated soil at a depth of approximately 20–30 cm. We used the shaking method [19] to remove excess soil, and collected rhizosphere soil that was tightly attached to the roots within 0–2 mm. The collected soil samples were divided into two parts: one was placed into 10 mL centrifuge tubes and stored in a −80 °C freezer for subsequent DNA extraction and high-throughput sequencing; the other was air-dried at room temperature, and then ground and sieved through a standard sieve (pore size of 0.25 mm) for subsequent determination of soil physicochemical properties and enzyme activities.

2.3. Determination of Soil Physicochemical Properties and Soil Enzyme Activity

The soil physicochemical properties were determined according to a previous study [20]. Soil pH was measured at a soil-to-water ratio of 2.5:1. The soil OM, TN, TP, and TK contents were determined using the potassium dichromate volumetric, Kjeldahl, hydrofluoric acid–high chloric acid digestion–molybdenum antimony colorimetric, and hydrofluoric acid–high chloric acid digestion–flame photometry methods, respectively. The activities of soil hydrogen peroxide enzymes, urease, phosphatase, and sucrase were determined using the potassium permanganate titration, phenol-sodium hypochlorite colorimetric, phosphoric acid phenanthroline sodium colorimetric, and 3,5-dinitrosalicylic acid colorimetric methods, respectively. All measurements were repeated thrice.

2.4. DNA Preparation and Sequencing

The soil samples were filtered through a 2 mm sieve, and the total microbial genomic DNA was extracted using the CTAB method [21]. The concentration and quality of the DNA were determined by NanoDrop2000, and 1% agarose gel electrophoresis, respectively. For soil bacteria, the V4 region of the 16S rDNA was amplified using the primers 515F (5′-GTGCCAGCMGCCGCGGTAA-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-3′). For fungi, the ITS-5F region of the rRNA gene was amplified using the primers ITS5-1717F (5′-GGAAGTAAAAGTCGTAACAAGG-3′) and ITS2-2043R (5′-GCTGCGTTCTTCATCGATGC-3′) [22]. The amplification system (30 µL) consisted of Phusion Master Mix (2×) 15 µL, forward primer (0.2 µM/µL) 1 µL, reverse primer (0.2 µM/µL) 1 µL, gDNA (1 ng/µL) 10 µL, and ddH2O 2 µL. The amplification program included pre-denaturation at 98 °C for 1 min, followed by 30 cycles of denaturation at 98 °C for 10 s, annealing at 50 °C for 30 s, extension at 72 °C for 30 s, and the final extension was performed at 72 °C for 5 min. The PCR products were detected on a 2% agarose gel and then purified using an AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, USA) and quantified using QuantiFluor™-ST (Promega, Madison WI, USA). The purified amplicons were prepared in 2 × 300 PE libraries according to the standard operating procedure of the Illumina MiSeq platform (Illumina, San Diego, CA, USA). Finally, sequencing was performed using the Illumina MiSeq platform (Microbial Genomics, Shenzhen, China).

2.5. High-Throughput Sequencing and Raw Data Analysis

The software QIIME2 (2019.4 version) was used to analyze microbial communities following the official guidelines (https://docs.qiime2.org/2019.4/tutorials/, accessed on 1 August 2023). First, the raw sequence data were demultiplexed using the Demux plugin and the primers were trimmed with the Cutadapt plugin. Then, quality filtering, denoising, merging, and chimera removing of the sequences were performed using the DADA2 plugin [23]. Next, we integrated the obtained sequences based on 100% similarity to generate the feature sequence ASVs and abundance data tables. After comparing with the reference sequences in the Greengenes database (Greengenes (13_8)) [24], the ASVs with an abundance of less than 0.001% were removed in all samples, and the rest were further analyzed with the abundance matrix. Bar chart analysis was also conducted using the R software (ggplot2_3.4.4) to visually compare the differences in the number of ASVs and classification status among different samples at the phylum and genus levels. The relationships between the microbial and fungal community structures in the soil and physicochemical factors were analyzed using redundancy analysis (RDA) and Spearman’s correlation heat maps [25].

2.6. Statistical and Bioinformatics Analyses

Date of soil physicochemical properties and enzyme activities were processed and statistically analyzed using Excel 2010 and SPSS 25.0. One-way ANOVA and the least significant difference (LSD) tests multiple comparison analysis were utilized to assess the impact of different planting years on the soil microbial community diversity. Alpha diversity indices were calculated using QIIME2 2019.4 version, and their differences were evaluated using t-tests. Principal coordinate analysis (PCoA) was used based on Bray–Curtis dissimilarity to visualize changes in microbial community structure between different samples. Bar charts at the phylum and genus levels were created using R software to visually compare the number of classification units in different samples. The relationships between soil microbial community structures and physicochemical properties were analyzed using RDA and Spearman’s correlation heat maps.

3. Results

3.1. Effects of Different Planting Years on Rhizosphere Soil Physicochemical Properties

Significant differences were discovered in the soil properties among the different years of planting (p < 0.05) (Table 1). Soil pH significantly decreased with increasing planting years (p < 0.05), while the OM content gradually improved and reached to a significant level at 6 and 10 years after planting C. humilis. The nutrient content in the rhizosphere soil of C. humilis planted for 3 years was significantly lower than that of other planting years (p < 0.05), and the AN and TN content in the rhizosphere soil of C. humilis planted for 6 years was the highest. The TP, TK, AP, and AK contents in the rhizosphere soil of C. humilis planted for 10 years were significantly higher than those in the other planting years (p < 0.05).

3.2. Effects of Different Planting Years on Rhizosphere Soil Enzyme Activity

After planting C. humilis, enzyme activities of alkaline phosphatase, urease, sucrase and catalase in the rhizosphere soil was significantly improved compared to the control (p < 0.05) and all peaked at 6 years of C. humilis planting (Table 2). Notably, the enzyme activities of all four enzymes significantly decreased at 10 years of C. humilis planting (p < 0.05).

3.3. Effects of Planting Years on Rhizosphere Soil Microbial Community Characteristics

3.3.1. Alpha Diversity and PCoA Analyses

The coverages of samples were all greater than 0.99 (Table 3, Figure S2), representing that the sequencing depth of samples could reflect the diversity of microbial communities. The Ace and Chaol indices were used to evaluate the richness of the microbial species in the samples, while the Shannon and Simpson indices were used to evaluate the diversity of the microbial species in the samples. For rhizosphere soil bacteria, the Chao1 and Ace indices were significantly improved compared to the control (p < 0.05), suggesting that C. humilis planting increased the richness of rhizosphere bacteria significantly. However, the Shannon index was significantly improved at 3 and 10 years of planting C. humilis, while the Simpson indices was basically unchanged, suggesting that the diversity of rhizosphere bacteria was less affected than the bacteria richness. For rhizosphere soil fungi, the Shannon and Simpson indices were significantly improved compared to the control (p < 0.05), suggesting that C. humilis planting increased the diversity of rhizosphere fungi significantly. The Ace and Chao1 indices firstly significantly decreased at 3 years and then increased at 6 and 10 years of C. humilis planting, suggesting that the richness of rhizosphere fungi was less affected than the bacteria diversity. Therefore, the differences of microbial communities among rhizosphere soil of 3, 6 and 10 years of C. humilis planting were contributed most by the bacteria richness and fungi diversity (Table 3).
The PERMANOVA analysis based on Bray–Curtis variance revealed that the planting years had a significant impact on the diversity of bacteria (F = 14.362, p = 0.001) and fungi (F = 11.379, p = 0.001) in the rhizosphere soil (Figure 2). As for soil bacteria (Figure 2a), the PC1 and PC2 contributed 60.57% and 16.53% of the total variation, respectively. Scatter plots showed samples of 3a_RC, 6a_RC, and 10a_RC were separated from the CK, respectively, which indicated that planting years had a significant impact on the structure of soil bacterial communities (p < 0.01). As for soil fungi (Figure 2b), revealed that the PC1 and the PC2 contributed 45.96% and 19.14% of the total variation, respectively. Scatter plots showed samples of 3a_RC, 6a_RC, and 10a_RC were separated from the CK, respectively, which indicated that planting years also had a significant impact on the structure of soil fungal communities (p < 0.01).

3.3.2. Microbial Community Composition and Structure

From the ASV feature sequences obtained, we identified the top 20 species based on their abundance and classified them in detail at the phylum and genus levels. At the level for bacteria (Figure 3a), the bacteria phylum with an average abundance greater than 1% were as follows: Proteobacteria, Actinobacteria, Acidobacteria, Gemmatimonadetes, Crenarchaeota, Chloroflexi, Bacteroidetes, Planctomycetes, Verrucomicrobia, and Nitrospirae. The relative abundance of rhizosphere soil bacterial compositions varied across different planting years, and the top three phyla with the highest relative abundances were Proteobacteria, Actinobacteria, and Acidobacteria, respectively. However, with an increase in planting years, the relative abundance of Proteobacteria first increased and then decreased, whereas the relative abundances of Actinobacteria and Acidobacteria gradually increased. We also observed that compared to the CK, the rhizosphere of C. humilis had a lower relative abundance of Gemmatimonadota, Chloroflexi, and Crenarchaeota (Table S1).
At the level for bacteria (Figure 3b), the bacteria genii with an average abundance greater than 1% were as follows: Candidatus_Nitrososphaera, Kaistobacter, Rhodoplanes, Steroidobacter, Sphingomonas, Arthrobacter, Rubrobacter, Skermanella and Streptomyces. The top three genera with the highest relative abundance were Nitrososphaera, Kaistobacter, and Sphingomonas, accounting for approximately 23.12–37.41% of the total bacteria. Compared to the CK, the relative abundance of Nitrososphaera was decreased in the rhizosphere soil of different planting years. The relative abundances of Kaistobacter in the CK, 3a_RC, 6a_RC and 10a_RC were 3.02%, 4.49%, 6.48%, and 5.23%, respectively, indicating an increasing trend with increasing planting years. The relative abundances of Sphingomonas were similar to Kaistobacter, which higher than CK and increased to varying degrees with increasing planting years (Table S2).
At the phylum level for fungi (Figure 3c), there were three phyla with an average abundance greater than 1% (Ascomycota, Basidiomycota, and Mortierellomycota). The relative abundance of Ascomycota gradually increased from the CK to the 10_RC, while the relative abundance of Mortierellomycota decreased from the CK to the 10_RC. However, the relative abundance of Basidiomycota was the highest in the CK, followed by 10a_RC, 3a_RC and 6a_RC (Table S3).
At the genus level for fungi (Figure 3d), three fungi genera (Mortierella, Solicoccozyma, and Neocosmospora) had an average abundance greater than 1%, which accounting for approximately 13.79–40.06% of the total fungi. Compared with the CK, the relative abundance of Mortierella, Solicoccozyma, and Neocosmospora of 3a_RC, 6a_RC and 10a_RC decreased, but compared with 3a_RC, the relative abundance of Solicoccozyma and Neocosmospora of 6a_RC increased (Table S4).

3.4. Correlation between Rhizosphere Microorganisms and Soil Physicochemical Properties

Correlation analysis between physicochemical properties and the dominant bacteria phyla (Figure 4a) revealed that the RDA1 and RDA2 contributed 33.19% and 21.81% of the total variation in the bacterial communities, respectively. The separation of Actinobacteria, Acidobacteria, and Proteobacteria along the first RDA axis was mainly influenced by AK, AP, TP, and pH. The structure of the Acidobacteria communities was associated with higher TP and lower pH values. The influence of soil physicochemical properties on the bacterial community structure was ranked as follows: AK > AP > TP > pH > TK > AN > TN > OM.
Correlation analysis between physicochemical properties and the dominant fungi phyla (Figure 4b) revealed that the RDA1 and RDA2 contributed 30.63% and 21.68% of the total variation in the fungi communities, respectively. The separation of Mortierellomycota, Basidiomycota and Ascomycota along the second RDA axis. The separation was predominantly influenced by TK, AK, and pH. The structure of Ascomycota communities was correlated to higher AK, TK and lower pH values. The influence of soil physicochemical properties on the fungal community structure was ranked as follows: TK > OM > AK > pH > TP > TN > AN > AP.
To better understand the relationship between soil microorganisms and soil physicochemical indicators in C. humilis during different planting years, we selected the top 10 bacterial and fungal genera, and a correlation clustering heatmap analysis was then conducted (Figure 5). The analysis revealed that the abundance and distribution of bacteria were mainly influenced by pH, TP, TK, AK, and AN (Figure 5a). Actinobacteria and Gemmatimonadetes were significantly positively correlated with pH, whereas they were significantly negatively correlated with TP, TK, and AK (p < 0.01). AP was significantly negatively correlated with Crenarchaeota and Firmicutes and significantly positively correlated with Actinobacteria and Planctomycetes (p < 0.05). Proteobacteria were significantly correlated with AN and TN (p < 0.05). Moreover, compared to bacteria, fungi were more susceptible to soil nutrient contents, such as pH, N, P, K, and OM (Figure 5b). Further analysis revealed that Cercozoa and Ascomycota were significantly positively correlated with TK (p < 0.01) and significantly negatively correlated with pH (p < 0.01); however, Aphelidiomycota and Mortierellomycota were significantly negatively correlated with TK (p < 0.05) and significantly positively correlated with pH (p < 0.01). We also observed a significant positive correlation between OM and Cercozoa and Ascomycota (p < 0.01), whereas there was a significant negative correlation between OM and Aphelidiomycota (p < 0.001).

4. Discussion

4.1. Impact of Planting Year on the Physicochemical Properties and Enzyme Activity of Rhizosphere Soil in C. humilis

Previous studies have shown that cultivating C. humilis can improve soil structure, soil fertility, and enzyme activity [18,26]. The results of this study indicated that soil pH decreases with increasing planting years, suggesting that cultivating C. humilis can improve alkaline soil and reduce soil pH. The improvement effect is positively correlated with planting years, and similar results have been obtained in the research on planting alfalfa (Medicago sativa L.) in saline–alkali soil for several years [27]. This study also showed that the TN and alkali–hydrolyzable nitrogen in the soil increased significantly until 6 years and decreased after 10 years. Therefore, it is necessary to properly add nitrogen fertilizer during the long-term planting of C. humilis. In addition, the contents of AK, TP, TK, and OM in the rhizosphere soil significantly increased with increasing planting years. However, the content of AP showed a decreasing trend after three years, which may be related to the higher demand for AP by C. humilis in the early growth stage. In summary, with an increase in the planting years of C. humilis, most of the soil’s physicochemical properties gradually developed in a favorable direction.
Soil enzyme activities are crucial indicators for assessing soil fertility, quality, and health status [28]. For instance, soil urease can convert organic nitrogen into inorganic nitrogen, improving the nitrogen supply for plants [29], which aligns with the trends of TN and alkali–hydrolyzable nitrogen in this study. Phosphatase catalyzes the hydrolysis of soil phosphate, and its activity is often used as an indicator of soil phosphate level [30]. Our study demonstrated that the activities of alkaline phosphatase, urease, sucrase, and catalase in the rhizosphere soil peaked at 6 years after C. humilis planting and then decreased at 10 years. The initial increase in alkaline phosphatase and sucrase levels may be related to root exudates [31], while the subsequent decrease at 10 years was partly due to the weakened nitrogen-fixing ability of aging C. humilis. Moreover, C. humilis has an extensive root network that can absorb nutrients from the deeper soil layers [32,33]. Peroxidase in the soil acts as a key biological catalyst, efficiently converting hydrogen peroxide into water and oxygen, and plays a crucial role in maintaining soil ecological balance [34]. However, with an increase in the planting years of C. humilis, the significant decline in peroxidase activity may lead to an increase in hydrogen peroxide concentration in the soil, potentially affecting the soil structure and biological survival. This decrease in enzyme activity indicates a significant relationship between soil health and planting patterns [35]. Therefore, for future long-term planting of C. humilis, the proper application of biochar should be considered to enhance soil enzyme activity.

4.2. Impact of Planting Year on the Characteristics of Rhizosphere Soil Bacterial Community in C. humilis

Perennials could affect the community structure and distribution of soil microorganisms by releasing root exudates [36,37]. Planting year also affects the diversity and composition of microorganisms in the soil surrounding the roots [38,39]. Some researchers reported a continuous decrease in microbial diversity as planting years increased [5,40]. However, in this study, as the year of planting C. humilis increased, the richness and diversity of rhizosphere bacteria also increased. Similar results have been observed in the long-term cultivation of Macadamia integrifolia [41]. We speculated that as C. humilis plants age, their expanded root systems secrete more exudates, which change the acid–alkaline environment (low pH) to obtain more sugars, amino acids, and organic acids from the root exudates. Therefore, changes of the root exudates in different planting years can lead to alterations in the composition of rhizosphere microbial communities directly or indirectly by modifying the soil micro-environment [42,43,44,45,46].
In this study, we observed significant differences in the structure and relative abundance of bacterial communities among C. humilis during different planting years. At the phylum level, Proteobacteria, Actinobacteria, and Acidobacteria are three dominant phyla in the rhizosphere soil, which aligns with previous studies [47,48]. Proteobacteria are a class of bacteria found in various plant roots capable of degrading OM and promoting crop growth [49]. This might be due to the fact that Proteobacteria, as Gram-negative bacteria, have outer membranes primarily composed of lipopolysaccharides (LPS), which offer good protection for rRNA [50]. As a result, Proteobacteria can adapt to most environmental conditions and become the dominant bacterial phylum in the rhizosphere of plants [51]. However, in this study, the proportions of Proteobacteria in the CK, 3-, 6-, and 10-year samples were 26.10%, 28.36%, 34.92%, and 20.15%, respectively, showing an initial increase, then decreased with increasing planting years. Hence, for long-term planting C. humilis, it is necessary to properly apply microbial fertilizer to the soil. Actinobacteria are involved in the global carbon cycle and decomposition of OM, serving as a major source of soil nutrients and are widely present in soil microbial communities. Their presence can help prevent most soil-borne diseases [52]. In this study, the richness of Actinobacteria decreased after 3 years and then increased, which may be related to the underdeveloped rhizosphere in the early stage of C. humilis. As the planting years increased, the roots gradually developed and disease resistance improved. Acidobacteria are a group of bacteria capable of degrading lignin and fiber components, providing abundant energy to microorganisms in the rhizosphere ecosystem after degradation. The study’s results indicated that that the proportion of Acidobacteria increased with the number of planting years of C. humilis.
At the genus level, Nitrososphaera, Kaistobacter, and Sphingomonas are the three dominant genera of C. humilis rhizosphere soil. Nitrososphaera has been confirmed as an ammonia-oxidizing archaeon which could transform ammonia into nitrite [53]. In our study, the relative abundance of Nitrososphaera decreased, which indicated the planting of C. humilis could alter the process of nitrogen transformation. Previous studies have identified Kaistobacter as a dominant genus in healthy rhizospheric soil [52]. It was found that the relative abundance of Kaistobacter increased after planting C. humilis, indicating a positive change in rhizospheric soil health of C. humilis. Sphingomonas plays a role in nitrogen fixation, denitrification, and reducing soil toxicity [54]. Our findings revealed that the relative abundance of Sphingomonas increased in the early stages of planting C. humilis, indicating an improvement in the rhizospheric soil environment and enhanced overall health conditions. However, after 10 years of planting C. humilis, the relative abundance of Sphingomonas decreased, possibly due to microbial ecological imbalance in the long-term continuous planting of C. humilis. In addition, this study found that with increasing planting years, the species richness (Ace, Chao1) and diversity (Shannon, Simpson) of the soil bacterial community in the rhizosphere of C. humilis also increased.

4.3. Impact of Planting Year on the Characteristics of Rhizosphere Soil Fungal Community in C. humilis

Fungi play a key role in decomposing soil organic matter, making them an essential part of soil ecosystems [3,55]. We discovered that long-term C. humilis planting can change the structures of the soil fungal community. The three most abundant fungal phyla in all soil samples were Ascomycota, Basidiomycota, and Mortierellomycota, which is consistent with previous research [56,57]. Ascomycota can tolerate pressure conditions, such as low nutrient availability [58]. In this study, the relative abundance of Ascomycota increases with the number of planting years, possibly due to the decrease in soil nutrient content caused by long-term continuous planting. Basidiomycota can establish a symbiotic relationship with plants and break down wood and fibers [59,60,61]. The results of this study showed that the Basidiomycota abundance increased from 3 to 10 years after C. humilis planting, which aligns with previous studies [62]. Mortierellomycota mainly includes saprophytic fungi in the soil and has a good inhibitory effect on plant pathogens, such as wilt and root rot [35]. The relative abundance of Mortierellomycota decreased with continuous planting, possibly due to the disruption of the microbial community balance [63].
Three dominant genera Mortierella, Solicoccozyma, and Neocosmospora were identified in the rhizosphere soil of C. humilis. Mortierella is a beneficial fungus that is commonly found in soil and helps promote crop growth and disease resistance [57,63]. Previous research has shown that Mortierella plays a crucial ecological role in the degradation of polycyclic organic matter in the soil, thereby could enhance crop growth [64]. However, in this study, there was a significant decrease in the relative abundance of Mortierella with increasing planting years indicating an imbalanced microbial environment of long-term planting of C. humilis. The underlying mechanism requires further investigation. Solicoccozyma belongs to the Bacillaceae family and can produce external toxins that inhibit other pathogens [65]. Previous studies have also found that Solicoccozyma could effectively promote plant growth by influencing soil enzyme activities [65]. In this study, we observed a slight increase in the relative abundance of Solicoccozyma after 6 years of planting, possibly due to the peaked soil enzyme activities. However, from 6 years to 10 years of planting C. humilis, the relative abundance of Solicoccozyma gradually decreased. Neocosmospora, a newly discovered fungus, has been identified as a pathogen causing root rot in many field crops [66]. Planting C. humilis effectively reduced the occurrence of Neocosmospora in this study, which may be partly attributed to the increased nitrogen content during continuous planting of C. humilis. Furthermore, the relative abundances of some beneficial microbes decreased after long-term planting of C. humilis, which means subsequent application of microbial fertilizers may be needed.

4.4. Correlation between Soil Physicochemical Properties and Rhizosphere Microbial Community Characteristics

The growth of plants, the physicochemical properties of soil, nutrient levels, and rhizosphere microorganisms are closely related and have a significant mutual influence [67]. The composition of microbial communities is influenced by pH and soil nutrients (such as C, N, and P content) and is correlated with soil health, which further affects plant growth [14]. Similarly, soil microorganisms can influence soil physicochemical properties [68]. In this study, significant correlations were found between soil physicochemical properties and rhizosphere microbial communities (Figure 4 and Figure 5). The RDA results indicated that OM, pH, AK, and TK had significant effects on the diversity of bacterial and fungal communities. pH was positively correlated with Proteobacteria, Gemmatimonadota, Ascomycota, and Basidiomycota, but negatively correlated with Actinobacteria and Acidobacteria, which is consistent with previous findings [45]. The results also showed that planting C. humilis increased the diversity of microbial communities and improved soil quality. Soil pH significantly decreased, whereas AK, AP, and OM contents significantly increased during the 10-year planting period of C. humilis. This improvement may be attributed to the vigorous activity of the rhizosphere microorganisms [69].
It was also reported soil fungal communities are more sensitive to the soil physicochemical properties than bacterial communities [70]. In the rhizosphere soil of C. humilis at different planting years, most of the fungal members were significantly affected by pH, N, P, K, and OM. However, most of the bacteria members were less influenced. Additionally, we believe that changes in the structure of microbial communities in the rhizosphere of C. humilis are not only linked to changes in soil physicochemical properties after continuous planting, but may also be associated with the accumulation of root exudates or residues; therefore, the effects of root exudates on the structure of microbial communities in the rhizosphere of C. humilis need to be studied.

5. Conclusions

This study revealed how C. humilis planted for a variable number of years (3, 6, and 10 years) affected rhizosphere soil physicochemical properties, enzymes, and microbial communities. Planting C. humilis significantly reduced the pH value of the rhizosphere soil, while the OM, TP, TK, and soil enzyme activities showed an overall increasing trend. Correlation analysis revealed that AK and TK were the most important factors influencing bacteria and fungi communities in the rhizosphere soil of C. humilis, respectively. Furthermore, the relative abundance of beneficial bacteria (Acidobacteria, Proteobacteria, Actinobacteria), and beneficial fungi (Ascomycota, Mortierellomycota, and Basidiomycota) increased in the rhizosphere soil of C. humilis after long-term planting. Taken together, this study provides a basis for further studies on the ecological improvement effects and sustainable cultivation of C. humilis.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae10101102/s1. Figure S1 Soil sample. Note: The naming of each sample in the table is the same as that in Table S1. Figure S2 Rarefaction curves observed-features in soil sample. (A): Rarefaction curves of bacteria; (B): Rarefaction curves of fungi. Table S1 Relative abundance of rhizosphere soil bacterial communities at the phylum level. Table S2 Relative abundance of rhizosphere soil bacterial communities at the genus level. Table S3 Relative abundance of rhizosphere soil fungal communities at the phylum level. Table S4 elative abundance of rhizosphere soil fungal communities at the genus level.

Author Contributions

Conceptualization, X.M. (Xiaopeng Mu); methodology, J.W. and H.Q.; formal analysis, J.D.; investigation, S.Z. and J.Z.; resources, P.W.; writing—original draft preparation, J.W.; writing—review and editing, X.M. (Xiaopeng Mu); supervision, X.M. (Xiaoyan Mou), L.W. and S.L.; project administration, X.M. (Xiaopeng Mu). 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 of China Youth Fund, grant number 32101648, and the Shanxi Agricultural University 2019 Science and Technology Innovation Doctoral Research Start-up Fund Project, Grant No. 2018YJ06.

Data Availability Statement

The original contributions presented in the study are included in the supplementary material, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Location map of the Cerasus humilis planting site in this study.
Figure 1. Location map of the Cerasus humilis planting site in this study.
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Figure 2. PCoA of rhizosphere soil bacterial (a) and fungal (b) community structure based on Bray–Curtis results. Note: 3a_RC, 6a_RC, and 10a_RC represented rhizosphere soil of Cerasus humilis planted for 3, 6 and 10 years, respectively.
Figure 2. PCoA of rhizosphere soil bacterial (a) and fungal (b) community structure based on Bray–Curtis results. Note: 3a_RC, 6a_RC, and 10a_RC represented rhizosphere soil of Cerasus humilis planted for 3, 6 and 10 years, respectively.
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Figure 3. Relative abundance of Cerasus humilis rhizosphere soil microbial communities at phylum and genus levels in different planting years. Note: (a,b) represent bacteria abundance at the phylum and the genus level, respectively; (c,d) represent fungi abundance at the phylum and the genus level, respectively.
Figure 3. Relative abundance of Cerasus humilis rhizosphere soil microbial communities at phylum and genus levels in different planting years. Note: (a,b) represent bacteria abundance at the phylum and the genus level, respectively; (c,d) represent fungi abundance at the phylum and the genus level, respectively.
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Figure 4. RDA analysis of Cerasus humilis rhizosphere soil at 10 dominant bacterial (a) and fungal (b) phylum and soil factors. Note: pH, TN, TP, TK, AN, AP, AK, and OM represent the pH value, total nitrogen, total phosphorus, total potassium, available nitrogen, available phosphorus, available potassium, and soil organic matter, respectively.
Figure 4. RDA analysis of Cerasus humilis rhizosphere soil at 10 dominant bacterial (a) and fungal (b) phylum and soil factors. Note: pH, TN, TP, TK, AN, AP, AK, and OM represent the pH value, total nitrogen, total phosphorus, total potassium, available nitrogen, available phosphorus, available potassium, and soil organic matter, respectively.
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Figure 5. Correlation heat map of Cerasus humilis rhizospheric soil at 10 dominant bacterial (a) and fungal (b) phyla with soil factors. Note: pH, TN, TP, TK, AN, AP, AK, and OM represent the pH value, total nitrogen, total phosphorus, total potassium, available nitrogen, available phosphorus, available potassium, and organic matter, respectively. * p < 0.05, ** p < 0.01, *** p < 0.001.
Figure 5. Correlation heat map of Cerasus humilis rhizospheric soil at 10 dominant bacterial (a) and fungal (b) phyla with soil factors. Note: pH, TN, TP, TK, AN, AP, AK, and OM represent the pH value, total nitrogen, total phosphorus, total potassium, available nitrogen, available phosphorus, available potassium, and organic matter, respectively. * p < 0.05, ** p < 0.01, *** p < 0.001.
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Table 1. Effects of different planting years on Cerasus humilis rhizosphere soil physicochemical properties.
Table 1. Effects of different planting years on Cerasus humilis rhizosphere soil physicochemical properties.
IndexCK3a_RC6a_RC10a_RC
pH8.47 ± 0.33 a8.03 ± 0.33 b7.73 ± 0.09 c7.43 ± 0.03 d
Available N (mg/kg)58.03 ± 1.86 c93.96 ± 1.46 b119.74 ± 1.46 a61.10 ± 1.07 c
Available P (mg/kg)9.70 ± 0.34 bc8.96 ± 0.37 c10.30 ± 0.82 ab16.89 ± 0.39 a
Available K (mg/kg)79.08 ± 2.34 d180.761 ± 3.64 c194.82 ± 2.43 b271.02 ± 2.22 a
Total N (g/kg)0.87 ± 0.06 d1.37 ± 0.06 b1.73 ± 0.10 a1.10 ± 0.06 c
Total P (g/kg)0.49 ± 0.01 d0.67 ± 0.01 c0.83 ± 0.02 b1.25 ± 0.01 a
Total K (g/kg)13.06 ± 0.38 d18.85 ± 0.30 c24.73 ± 0.91 b29.22 ± 0.13 a
Organic matter (g/kg)10.96 ± 0.54 c13.02 ± 0.89 c22.41 ± 0.64 b25.56 ± 0.15 a
Note: Data are presented as the means and standard error (n = 3). Different lowercase letters indicate significant differences at p < 0.05.
Table 2. Effects of different planting years on Cerasus humilis rhizosphere soil enzyme activities.
Table 2. Effects of different planting years on Cerasus humilis rhizosphere soil enzyme activities.
Soil Enzyme ActivityCK3a_RC6a_RC10a_RC
Alkaline phosphatase activity (mg/(g·d))0.75 ± 0.03 d1.07 ± 0.05 b1.47 ± 0.01 a0.96 ± 0.01 c
Urease activity (mg/(g·d))0.67 ± 0.01 c0.93 ± 0.02 b1.06 ± 0.00 a0.95 ± 0.03 b
Sucrase activity (mg/(g·d))18.10 ± 0.61 d23.55 ± 1.58 c56.49 ± 0.31 a44.55 ± 0.77 b
Catalase activity (mg/(g·20 min))3.81 ± 0.03 d4.01 ± 0.07 c5.83 ± 0.10 a5.02 ± 0.03 b
Note: Data are presented as the means and standard error (n = 3). Different lowercase letters indicate significant differences at p < 0.05.
Table 3. Alpha diversity of Cerasus humilis soil microorganisms at different planting years.
Table 3. Alpha diversity of Cerasus humilis soil microorganisms at different planting years.
Planting YearsAceChao1ShannonSimpsonCoverage
BacteriaCK1712.23 c1715.71 c9.579 b0.997 a0.99 a
3a_RC2577.76 a2491.80 a10.045 a0.997 a0.99 a
6a_RC2162.85 b2178.74 b9.732 b0.996 a0.99 a
10a_RC2491.80 a2491.03 a10.127 a0.998 a0.99 a
FungiCK548.10 a543.23 a5.632 b0.926 b0.99 a
3a_RC493.58 b496.13 b6.226 a0.965 a0.99 a
6a_RC564.16 a563.21 a6.425 a0.969 a0.99 a
10a_RC568.78 a570.27 a6.438 a0.969 a0.99 a
Note: Data are presented as the means (n = 3). Different lowercase letters indicate significant differences at p < 0.05.
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Mu, X.; Wang, J.; Qin, H.; Ding, J.; Mou, X.; Liu, S.; Wang, L.; Zhang, S.; Zhang, J.; Wang, P. Analyses of Rhizosphere Soil Physicochemical Properties and Microbial Community Structure in Cerasus humilis Orchards with Different Planting Years. Horticulturae 2024, 10, 1102. https://doi.org/10.3390/horticulturae10101102

AMA Style

Mu X, Wang J, Qin H, Ding J, Mou X, Liu S, Wang L, Zhang S, Zhang J, Wang P. Analyses of Rhizosphere Soil Physicochemical Properties and Microbial Community Structure in Cerasus humilis Orchards with Different Planting Years. Horticulturae. 2024; 10(10):1102. https://doi.org/10.3390/horticulturae10101102

Chicago/Turabian Style

Mu, Xiaopeng, Jing Wang, Hao Qin, Jingqian Ding, Xiaoyan Mou, Shan Liu, Li Wang, Shuai Zhang, Jiancheng Zhang, and Pengfei Wang. 2024. "Analyses of Rhizosphere Soil Physicochemical Properties and Microbial Community Structure in Cerasus humilis Orchards with Different Planting Years" Horticulturae 10, no. 10: 1102. https://doi.org/10.3390/horticulturae10101102

APA Style

Mu, X., Wang, J., Qin, H., Ding, J., Mou, X., Liu, S., Wang, L., Zhang, S., Zhang, J., & Wang, P. (2024). Analyses of Rhizosphere Soil Physicochemical Properties and Microbial Community Structure in Cerasus humilis Orchards with Different Planting Years. Horticulturae, 10(10), 1102. https://doi.org/10.3390/horticulturae10101102

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