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Article

Effect of Vermicompost Application on the Soil Microbial Community Structure and Fruit Quality in Melon (Cucumis melo)

by
Mei Tian
1,
Rong Yu
1,
Song Guo
1,
Wanbang Yang
1,
Shengfeng Liu
1,
Huiying Du
1,
Jinjin Liang
2,* and
Xingxu Zhang
2,*
1
Institute of Horticulture, Ningxia Academy of Agricultural and Forestry Sciences, Yinchuan 750002, China
2
State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(11), 2536; https://doi.org/10.3390/agronomy14112536
Submission received: 22 September 2024 / Revised: 19 October 2024 / Accepted: 25 October 2024 / Published: 28 October 2024
(This article belongs to the Special Issue Humic Substances: Chemistry and Multidimensional Role in Agricultural Systems and Pollution Management)
Browse Figures
Versions Notes

Abstract

:
Melon (Cucumas melon) is widely cultivated and popular because of its quality value and unique flavor. However, the continuous cropping of melons in greenhouses has various negative effects on the soil environment, melon growth, and quality. Recently, farmers have utilized organic fertilization, especially vermicompost, for melons to resist the harmful effects of continuous cropping. A field experiment was conducted to explore the effects of vermicompost on soil microbes and melon fruit quality via high throughput sequencing and chemical sequencing methods. The results showed that the application of vermicompost decreased (p < 0.05) soil pH and increased organic matter, available phosphorus, biomass, urease, catalase, peroxidase, and alkaline phosphatase. A total of 3447 bacterial and 718 fungal operational taxonomic units were identified in all soil samples. Application of vermicompost decreased (p < 0.05) the relative abundances of Acidobacteriota, Gemmatimonadota, Actinobacteriota, and unclassified and increased the relative abundance of Planctomycetota. Compared with the control soil, vermicompost application resulted in significantly higher bacterial Chao indices and a significantly lower Chao index under vermicompost of 60 t ha−1 based on farmers’ normal fertilizer and significantly lower diversity under vermicompost of 90 t ha−1. Otherwise, vermicompost application increased the photosynthetic rate and chlorophyll content of melon leaves and increased the total sugar, soluble solids, vitamin C, soluble protein, and organic acid contents of melon. The results of redundancy analysis indicated that Proteobacteria exhibited a positive correlation with soil ammonium nitrogen (AN) and pH, while showing a negative association with soil available phosphorus and organic matter. Spearman’s correlation analysis revealed that both total sugar content and central soluble solid content in melon had a significant positive correlation (p < 0.05) with Patescibacteria. This study demonstrates that the application of vermicompost alters the microbial community structure in melon cultivation, enhancing fruit quality; this not only promotes a healthier soil ecosystem but also contributes to sustainable and productive practices in melon farming.

1. Introduction

Melon (Cucumas melon) is widely cultivated and popular because of its quality value and unique flavor [1]. It belongs to the Cucurbitaceae family, which comprises 130 genera, including approximately 800 species, and is mainly found in temperate, subtropical, and tropical regions worldwide [2]. In the past decades, studies on melons have focused on breeding varieties in China and other countries, including the USA, Republic of Korea, Iran, and Turkey [3]. China is the largest producer of melons, possessing a wealth of genetic resources [4,5]. Notably, melon cultivation has significantly contributed to economic development by enabling farmers in the Ningxia Hui Autonomous Region to improve their livelihoods and alleviate poverty [6].
Melons are increasingly continuously planted in greenhouses to improve quality, harvest time, and yield [7]. However, continuous melon cropping negatively affects the soil environment, melon growth, and quality [8]. In particular, the soil microbial community has an indispensable effect on maintaining the health and stability of soil ecosystems and the structural imbalance of soil microbial communities is an essential factor in the continuous cropping of melon obstacles [9]. A previous study showed that continuous cropping reduced the soil bacterial diversity but increased the soil pathogenic fungi [10]. Many methods have been applied to solve continuous cropping obstacles, such as crop rotation [11], soil sterilization [12], grafting technology [13], and the application of organic fertilizers [14,15]. As a green, sustainable method with no chemical pollution, applying organic fertilizer mitigated the yield constraints caused by continuous cropping management [16] and long-term application of organic fertilizer-balanced soil chemicals, including N (nitrogen), P (phosphorous), and K (potassium), to promote soil microbial biomass, diversity, and activity, thereby enhancing the growth and production of crops [17]. In conclusion, organic fertilization is an efficient method for resisting the harmful effects of continuous cropping.
Melons are one of the most important economic crops in the Ningxia Hui Autonomous Region of China. In recent years, melon production in Ningxia has rapidly increased, with the area of melon sown in Ningxia reaching approximately 10,380 hm2 in 2017 [7]. In the context of the continuous cropping of melon in Ningxia, utilizing organic fertilizer such as vermicompost rather than chemical fertilizer is essential for maintaining the ecology of the soil [18], improving the utilization efficiency of fertilizer [19], decreasing the severity of disease [20], and increasing the quality of melon [21,22]. A previous study illustrated that the utilization of organic fertilizers could increase the richness of soil microbes, some of which are known to be involved in the degradation of complex organic compounds, such as manure and compost [23,24]. One organic fertilizer, vermicompost plays a key role in the organic cultivation of melon crops [15] and is increasingly recognized. Vermicompost is highly important, playing an essential role in remising obstacles caused by the continuous planting of melons. However, there is a lack of research on the impact of vermicompost on the chemical properties of soil and microorganisms of earthworm castings.
This study aims to elucidate the effects of vermicompost application on soil microbial diversity and subsequent fruit quality in melon cultivation. We conducted experiments with melons under four different fertilization gradients in the Ningxia Hui Autonomous Region of China. Soil microbial communities, chemical properties, and melon quality were analyzed using high-throughput sequencing and chemical assays, respectively, to assess the impact of vermicompost on soil microbial community structure and fruit quality in melons.
We hypothesized that the use of vermicompost would (1) alter soil chemical properties; (2) modify the composition of bacterial and fungal communities; and (3) enhance photosynthetic activity, thereby improving melon quality.

2. Material and Methods

2.1. Site Description and Experimental Design

The research was conducted in field plots located in Haiyuan County, Zhongwei City, Ningxia Hui Autonomous Region, China (105°69′26.86″ E, 36°36′74.65″ N, altitude 1547 m). Haiyuan County features a continental monsoon climate, with an average annual precipitation of 352.9 mm, evaporation of 1644.7 mm, and an average temperature of 7.7 °C. Precipitation is mainly concentrated from July to September.
The vermicompost application experiment was carried out in a large greenhouse. The raw materials of the earthworm manure were cow manure and straw pile, decomposed by No. 2 earthworms [25]. The pH value was 7.96 and the contents of total potassium, total phosphorus, total nitrogen, and organic matter (OM) were 3.22%, 1.14%, 1.78%, and 27.2%. The quantity of Bacillus subtilis was 246 million g−1.
In the experiment, melons were planted in a large arch shed. The experimental year was the third year of continuous cropping in this soil, following 2020 and 2021. We selected the “Flower Girl” melon variety in China because it is a key variety for local cultivation and is highly popular in the local consumer market. Four treatments were established in the experiment: control (conventional cultivation), T1 (increased application of vermicompost 30 t ha−1 based on farmers’ normal fertilizer), T2 (increased application of vermicompost 60 t ha−1 based on farmers’ normal fertilizer), and T3 (increased application of vermicompost 90 t ha−1 based on farmers’ normal fertilizer). The experiment had a completely randomized design, with three replicates per treatment. Plant spacing was 80 cm and row spacing was 60 cm [11]. The film was made of white polyethylene with a thickness of 0.008 mm and a width of 1.2 m. Melon seedlings with consistent growth were selected for planting and planted on 18 March 2022. During the growth period of the melons, fertilizer irrigation was carried out via drip irrigation and film-covered drip irrigation.

2.2. Sample Collection

Soil melon samples were collected on 30 August 2022. Five melon soil samples (200 g fresh weight) were randomly mixed as a sample with a total of three replicates for each treatment. The soil samples were quickly cooled using liquid nitrogen, brought back to the laboratory using dry ice, and stored at −80°C in a refrigerator before DNA extraction, microbial sequencing, and soil enzyme activity detection. For the detection of soil chemical properties, soil samples were sieved through a 2-mm sieve and stored at 4 °C in a refrigerator.
Melon samples (500 g fresh weight) were collected on 30 August 2022, and the melon yield was determined 22 times in total from 15 May to 30 August 2022.

2.3. Soil Chemical Properties Detection

Soil pH was measured at a 1:2.5 ratio in soil/water mixtures. Organic matter (OM) was analyzed using 0.25-mm sieved soil. Available potassium (AK) was assessed through the ammonium acetate method and flame photometry [26], while available phosphorus (AP) was determined using the molybdenum blue method [27]. Ammonium nitrogen (AN) was quantified with a continuous flow analyzer (FIAstar 5000 (FOSS, Hilleroed, Denmark)) [28]. Melon biomass was recorded as the total weight of the melons.

2.4. Soil Enzyme Activity Determination

Soil peroxidase (POD) activity was determined using the method described by [29] with guaiacol. Catalase (CAT) activity was determined using ultraviolet spectrophotometry, according to [30]. The urease (UE) activity was calculated as described by [31]. Sucrose (SC) activity was measured as described by [32]. Alkaline phosphatase (ALP) activity was calculated as described by [33].

2.5. DNA Extraction, Amplification, and Sequencing

Soil samples (0.1 and 0.5 g) were used to extract bacterial and fungal DNA with an MN NucleoSpin 96 soil DNA kit (Takara Bio USA, Inc., San Jose, CA, USA), following the manufacturer’s instructions. The bacterial 16S rRNA genes were amplified using the primers 335F (59-CADACTCCTACGGGAGGC-39) and 769R (59-ATCCTGTTTGMTMCCCVCRC-39). The internal transcribed spacer (ITS1) genes of the soil fungi were amplified using the primers ITS1F (59-CTTGGTCATTTAGAGGAAGTAA-39) and ITS2 (59-GCTGCGTTCTTCATCGATGC-39). PCR amplification was conducted in a total volume of 50 mL, comprising 10 mL of buffer, 0.2 mL of Q5 high-fidelity DNA polymerase, 10 mL of high GC enhancer, 1 mL of deoxynucleoside triphosphates, 10 mM of each primer, and 60 ng of genomic DNA. The cycling conditions included an initial step at 98 °C for 30 s, followed by 10 cycles of 98 °C for 10 s, 65 °C for 30 s, and 72 °C for 30 s, concluding with a final extension at 72 °C for 5 min.
High-throughput sequencing of bacterial and fungal rRNA genes was performed on purified pooled samples using the Illumina NovaSeq 6000 system at Biomarker Technologies Corporation (BMK) in Beijing, China. The processes of DNA detection, PCR amplification, and sequence analysis were all carried out by BMK.

2.6. Sequencing Data and Analyses of Diversity

The raw reads obtained were quality-checked and filtered to exclude those shorter than 20 bp. The remaining sequences, free of ambiguous bases, were assigned to OTUs with 97% identity using VSEARCH (v10.0) software. OTU identification was performed using Silva (release 128; http://www.arb-silva.de, 15 April 2024) for bacteria and Unite (release 7.2; http://unite.ut.ee/index.php, 15 April 2024) for fungi. The resulting OTU table was utilized to assess relative taxonomic abundances and conduct subsequent diversity analyses for both bacteria and fungi.
Alpha diversity indices, including the Chao, ACE, Shannon, and Simpson indices, were calculated using Mothur software (v.1.30) via their respective links (https://mothur.org/wiki/chao/, https://mothur.org/wiki/ace/, https://mothur.org/wiki/shannon/, https://mothur.org/wiki/simpson/, 15 April 2024).
For beta diversity analysis, principal coordinate analysis (PCoA) was employed, along with tests for significant differences in bacterial and fungal communities across treatments using analysis of similarity (ANOSIM) and permutational multivariate analysis of variance (PERMANOVA), based on Bray–Curtis dissimilarities, utilizing the vegan package in R (v.4.0.3).

2.7. Determination of Photosynthetic Index and Chlorophyll Content of Melon Leaves

The photosynthetic index and chlorophyll content of treated melon leaves were assessed prior to the first collection. Photosynthetic indices were measured using an LCpro T portable photo apparatus (ADC Company, Bristol, UK) with the light intensity set at 1500 Lx and temperature maintained at 25 ± 2 °C. The instrument was calibrated hourly, and readings were taken for the net photosynthetic rate, intercellular carbon dioxide concentration, transpiration rate, and stomatal conductance.
Chlorophyll content was determined with a handheld chlorophyll meter (SPAD-502 plus; Konica Minolta Sensing Company, Osaka, Japan). Leaves exhibiting similar photosynthetic indices were selected, and four measurements were taken for each using the chlorophyll analyzer. The average of these readings was recorded as the SPAD value for chlorophyll content. This value was then converted to specific chlorophyll content using the formula: Y(mg/dm2) = 0.0996X − 0.152, where X represents the seedling SPAD value and Y indicates the specific chlorophyll content of melon leaves.

2.8. Determination of Quality of Melon

The melon total sugar content and central soluble solids content were measured using a fruit sugar meter Sugar meter digital display sugar meter refractometer (Atto, Tokyo, Japan) [34,35,36,37]; vitamin C content was detected via titration and high-performance liquid chromatography [38]; melon soluble protein and organic acid were determined using liquid chromatography–mass spectrometry [39]. Soluble carbohydrate content was measured according to an abbe refractometer (Xylem, Washington, DC, USA) or sugar meter [40], and all indexes were calculated by the Ningxia Public Third Party Testing Co., Ltd. (Yinchuan, China).

2.9. Statistical Analyses

Differences in soil properties, bacterial and fungal communities, and diversities among treatments were analyzed using one-way ANOVA in SPSS 22.0 (SPSS Inc., Chicago, IL, USA). The least significant difference tests determined the statistical significance of mean differences, with a threshold set at p < 0.05. Additionally, the impact of varying vermicompost concentrations on soil bacterial and fungal communities was assessed using ANOSIM and PERMANOVA based on Bray–Curtis dissimilarities. Correlations between soil properties and microbial communities were measured using redundancy analysis (RDA) using CANOCO for Windows 4.5, and advanced Cor link correlations between soil microbial communities and melon qualities were performed via a heat map using R software (v.4.1.3) packages (ggplot2 3.3.3).

3. Results

3.1. Soil Chemical Properties and Enzyme Activity

Treatment with different vermicompost concentrations (p < 0.05) significantly affected soil pH (F = 4.31, p = 0.04), AK (F = 19.281, p = 0.001), biomass (F = 294.342, p = 0.000), SC (F = 19.281, p = 0.001), and POD (F = 9.157, p = 0.006) (Table 1). The pH decreased with the application of vermicompost, compared with the control. Compared with the control, the soil pH of T3 was significantly lower (p < 0.05) and there was no significant difference in soil pH between T2, the control, T1, and T3 (Table 1). T1 and T3 had significantly lower AK levels than the control but there was no significant difference between T2 and the control (Table 1). T3 had the highest biomass (p < 0.05), followed by T2, T1, and the control (Table 1). T2 had a significantly (p < 0.05) higher soil SC content than the other treatments. T1 had a significantly (p < 0.05) higher POD content than the control and T3 and there was no significant (p > 0.05) difference between T1 and T2 (Table 1).

3.2. Soil Bacterial and Fungal Taxon Compositions and Diversity

A total of 3447 bacterial and 718 fungal OTUs were identified across all soil samples at a 97% sequence similarity cut-off (Figure S1). The rarefaction curves for the 16S rRNA and internal transcribed spacer (ITS) gene sequences indicated that sequencing depths were adequate for all samples (Figure S2A,B).
At the phylum level, soil bacterial communities were primarily composed of Proteobacteria, Bacteroidetes, Acidobacteria, and Patescibacteria (Figure 1, Table S1). The relative abundance of Patescibacteria was significantly higher (p < 0.05) in T2 compared to the control and T3, while Planctomycetota was significantly lower (p < 0.05) in the control than in the other treatments.
For soil fungi, Ascomycota, Basidiomycota, and Rozellomycota dominated at the phylum level (Figure 2, Table S2). Ascomycota was significantly more abundant (p < 0.05) in T3 than in other treatments, whereas Basidiomycota was significantly higher (p < 0.05) in T2. Additionally, Mortierellomycota was significantly more abundant (p < 0.05) in T2 compared to other treatments, while Blastocladiomycota was significantly lower (p < 0.05) in T2. The relative abundance of unclassified taxa was significantly higher in the control and T1 than in T2 and T3 (Table S2).
For bacterial communities, T1 and T2 had a significantly higher Chao index of bacterial communities than the control and T3, while there was no significant difference between the control and T3 (Figure 3C). In addition, for fungal communities, the control and T1 had a significantly (p < 0.05) higher ACE index than T2 (Figure 3B). T3 had a significantly (p < 0.05) lower fungal diversity than the other treatments (Figure 3F,H). PCoA revealed that the soil microbial (containing bacterial and fungal) communities under treatment with different concentrations of vermicompost were significantly different (p < 0.05) among the control, T1, T2, and T3 (Figure 4 and Table 2).

3.3. Photosynthetic Index and Fruit Quality of Melon

Compared with the control, T1 had a significantly (p < 0.05) lower transpiration rate in melon leaves (Figure 5B). T1 had a significantly higher intercellular carbon dioxide concentration in melon leaves than the other treatments (Figure 5D). T2 had significantly (p < 0.05) higher total sugar, central soluble solid content, vitamin C, and organic acid content in melon than the other treatments; T3 had a significantly (p < 0.05) higher soluble carbohydrate content in melon than the other treatments (Table 3). Conventional cultivation with increasing application of vermicompost (60 t/hm2) is beneficial for cultivating melons. Photographs of melons treated with different concentrations of vermicompost are shown in Figure S3 and a detailed description of these photographs is provided in Table S3.

3.4. Relationship Between Soil Microbes and Soil Chemical Properties

The RDA analysis of soil bacterial communities, properties, and enzyme activity revealed that the first and second axes explained 33.63% and 27.52% of the variance, respectively. The length of each arrow indicates the contribution of the parameters to structural variation (Figure 6A). Notably, Proteobacteria showed a positive correlation with soil AN and pH, but a negative association with soil AP, ALP, POD, SC, UE, OM, and ACT. Bacteroidota was positively correlated with soil AK, POD, SC, UE, OM, and CAT, while negatively associated with soil AP, biomass, and AN (Figure 6A).
Similarly, the RDA for soil fungal communities, properties, and enzyme activity explained 49.2% and 21.33% of the variance, with arrow lengths representing parameter contributions to structural variation (Figure 6B). Ascomycota and Blastocladiomycota were positively correlated with soil UE, ALP, AP, biomass, AN, and CAT, but negatively correlated with OM, pH, POD, AK, and SC (Figure 6B).

3.5. Relationship Between Soil Microbes and Melon Quality

A total of 54 relationships were found between the relative abundance of soil bacterial phyla and melon quality, with 10 significant correlations (Figure 7A, Table S4). Total sugar and central soluble solid content were significantly (p < 0.05) positively correlated with Patescibacteria. The soluble protein content of melon was significantly (p < 0.05) positively correlated with Gemmatimonadota, organic acid was significantly (p < 0.05) positively correlated with Acidobacteria and Planctomycetota, and Vitamin C was significantly (p < 0.05) positively correlated with Acidobacteria, Patescibacteria, Planctomycetota, Gemmatimonadota, and Actinobacteria (Figure 7A, Table S4).
A total of 54 correlations were found between the relative abundance of soil fungal phyla and melon quality, with 18 of 54 significant correlations (Figure 7B, Table S5). The total sugar and central soluble solids contents of melon were significantly (p < 0.05) positively correlated with fungal Ascomycota, Basidiomycota, Mortierellomycota, Blastocladiomycota, and Calcarisporiellomycota. Vitamin C was significantly (p < 0.05) positively associated with Ascomycota, Basidiomycota, Mortierellomycota, and Blastocladiomycota. Soluble carbohydrate content was significantly (p < 0.05) positively correlated with Ascomycota, Rozellomycota, and Olpidiomycota. Organic acid was significantly (p < 0.05) positively associated with Blastocladiomycota (Figure 7B, Table S5).

4. Discussion

Soil properties, particularly chemical ones, are crucial in determining soil health [41]. Previous studies have shown that organic fertilizers, such as vermicompost, have a favorable impact on soil properties [42,43]; for instance, the application of vermicompost significantly enhances soil total organic carbon, total N, P, and K [44,45]. The application of vermicompost fertilizer increases soil available K and the biomass of crops [46,47] and reduces soil pH [48]. These results have significant implications for agricultural practices, especially in regions like the Ningxia Hui Autonomous Region, where high pH and salinized soils are common in melon-producing areas. By using vermicompost, farmers can improve soil health, enhance nutrient availability, and ultimately boost crop yields. The positive effects of vermicompost on soil properties emphasize its potential as a sustainable solution for addressing soil degradation and promoting agricultural productivity.
Previous studies have shown that vermicompost significantly alters the soil enzymatic activity [49,50]. Soil enzymes, such as urease, SC, catalase, peroxidase, and ALP, are essential soil fertility indices and originate from soil microorganisms [51]. As a hydrolase, urease is involved in crucial biological reactions in the carbon, nitrogen, and phosphorus [52]. Catalase is a product of metabolic and respiratory events that separate cytotoxic hydrogen peroxide from water and oxygen. Among the soil enzymes, urease, catalase, and phosphatase are prominent enzymes that have been the subject of many studies [53]. The activities of urease, phosphatase, and catalase in the host plant soil significantly increase with an increase in vermicompost concentration [54,55]. Vermicompost increases the microbial population in the soil, which in turn has a positive effect on the activity of soil urease, phosphatase, and catalase [56]. The results of the present study showed that the application of vermicompost significantly affected soil chemical properties such as pH and AK, and enzyme activity, including SC and POD. The application of vermicompost not only has positive effects on soil chemical properties and soil enzymatic activity in melon, but in other crops such as rice [57].
Regardless of whether organic or mineral fertilizer was utilized, soil bacterial communities mainly consisted of Proteobacteria and Bacteroidetes in melon soil [58]. Our findings align with a previous study indicating that, irrespective of the type of fertilizer—organic or mineral—soil bacterial communities in melon soils predominantly consist of Proteobacteria and Bacteroidetes. Notably, the application of vermicompost has been shown to markedly enhance the richness of these bacterial communities compared to mineral fertilizers [59]. Organic fertilizer improved the richness of the soil bacterial community and increased the relative abundance of the beneficial bacterial genera Flavobacterium, Bacillus, and Arthrobacter [60]. A similar study demonstrated that organic fertilizer promoted the relative abundance of beneficial bacteria, such as Acinetobacter, in melon plant soil [15]. The above studies illustrated that the application of organic fertilizer could alter bacterial communities. The results of the present study showed that the application of vermicompost significantly increased the relative abundance of Planctomycetota. The application of organic fertilizer increases the number of bacteria and Actinomycota in soil, decreases the incidence of Fusarium wilt disease, and increases melon yield [14]; as such, in light of these findings, it is evident that the strategic application of organic fertilizers, particularly vermicompost, can significantly alter soil bacterial communities in favor of beneficial organisms. This not only fosters a healthier soil ecosystem but also contributes to sustainable and productive melon farming practices.
The soil fungal communities of melons were dominated by Ascomycota and Basidiomycota, and the application of vermicompost significantly increased the relative abundances of Ascomycota, Basidiomycota, Rozellomycota, Mortierellomycota, and Blastocladiomycota. A previous study illustrated that the dominant fungal phyla in the soil for melon production are Ascomycota and Basidiomycota [61]. This study found that the soil fungal communities across the four treatments were predominantly composed of Ascomycota and Basidiomycota at the phylum level, with significant treatment effects on these communities. These findings align with previous research indicating that organic fertilizer application notably influences the richness and diversity of fungal communities in melon soil [15].
A previous study demonstrated that the application of vermicompost improved the microbial population in soil, which in turn increased the activity of soil urease, phosphatase, and catalase [56] because vermicompost provided additional substrates for the soil microbiota of crops, thus enhancing soil enzyme activity [62]. This study found that the dominant phylum Proteobacteria was positively associated with soil AN and pH, and other dominant phyla were positively or negatively correlated with soil properties and enzyme activity. Bacterial community composition was closely related to soil pH [63]. The relative abundance of Acidobacteria increases with lower pH [64]. Additionally, AN influences bacterial diversity in grassland soil microbial communities [65]. Nie et al. [66] found that high nitrogen levels decreased soil bacterial diversity and altered the composition of forest soil bacterial communities.
Ascomycota is strongly negatively correlated with soil pH and TN [67]. While this study also noted a negative correlation between Ascomycota and soil pH, previous research suggests that high pH can reduce soil fungal diversity. Although Ascomycota fungal communities were negatively correlated with soil pH in this study, this suppression could be explained by a previous study that revealed that high pH reduced soil fungal diversity [68]. Previous studies have shown that there are many important correlations between soil properties and soil microbes [11].
Previous studies have shown that the application of vermicompost increased plant growth [69,70], which was related to the present study that the application of vermicompost, on the one hand, increased the photosynthetic potential and growth of melon, improved the growth of plants, was conducive to the transformation, transportation, and distribution of photosynthetic organic products in melon leaves, prevented premature senescence, and prolonged the harvest period of melon, thus increasing the yield. It also had a positive effect on the chlorophyll content and quality of melon. The increase of soluble carbohydrate, vitamin, and soluble protein contents in fruit impacts the taste and commodity value of melon fruit.
Organic fertilizers improve the quality of plants due to increasing their high phenol, vitamin, total sugar, and polyamine contents [71]. However, organic fertilizers led to the formation of a new beneficial microbial community that suppressed Fusarium wilt [14]. Moreover, these bacteria were positively correlated with the sugar content in melon fruits [15]. Similarly, in the present study, the relative abundance of Patescibacteria was significantly positively correlated with total sugar and central soluble solid content, whereas the soluble protein content of melon was significantly positively correlated with Gemmatimonadota.
Overall, while vermicompost can offer significant benefits for soil health and crop productivity, careful management is crucial to avoid potential long-term negative effects related to nutrient saturation and pH shifts. Regular monitoring and adaptive management strategies can help sustain soil health and optimize cropping systems over time.

5. Conclusions

This study investigated the effects of vermicompost application on soil chemical properties, enzyme activity, and microbial communities, as well as chlorophyll content and melon quality. The results indicated that the application of vermicompost significantly decreased soil pH while increasing organic matter, available phosphorus, biomass, urease activity, catalase activity, peroxidase activity, and alkaline phosphatase levels compared to treatments without vermicompost.
Furthermore, the application of vermicompost led to a reduction in the relative abundances of Acidobacteriota, Gemmatimonadota, and Actinobacteriota while enhancing the relative abundance of Planctomycetota. In comparison to control soils, vermicompost application resulted in significantly higher bacterial Chao indices; however, a lower Chao index was observed under 60 t ha−1 treatment based on conventional fertilizer practices. Additionally, a decrease in diversity was noted under 90 t ha−1 treatment.
Moreover, the use of vermicompost enhanced both photosynthetic rates and chlorophyll content in melon leaves. It also increased total sugar content along with soluble solids, vitamin C levels, soluble protein concentrations, and organic acid contents in melons. This study provides theoretical support for the utilization of organic fertilizers for melon cultivation in the Ningxia Hui Autonomous Region of China.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14112536/s1, Figure S1. Venn diagram of soil bacterial (A) and fungal (B) OTUs; Figure S2. Rarefaction curves of the 16S rRNA and ITS gene sequence from the soil bacteria (A) and fungi (B) under different concentrations of earthworm droppings; Figure S3. Profile photographs of melon under the treatment of different concentrations of earthworm droppings; Table S1. Soil bacterial community composition at the phylum level; Table S2. Soil fungal community composition at the phylum level; Table S3. Charecteristic of “flower girl” (name of melon) under earthworm manure test in Haiyuan country; Table S4. Spearman’s correlation of advanced Cor link between bacterial relative abundance of soil and melon nutrition; Table S5. Spearman’s correlation of advanced Cor link between fungal relative abundance of soil and melon nutrition.

Author Contributions

Conceptualization, M.T.; Formal analysis, R.Y.; Funding acquisition, H.D. and S.L.; Investigation, S.G.; Methodology, R.Y. and M.T.; Project administration, S.L., H.D. and M.T.; Software, J.L.; Supervision, X.Z.; Validation, W.Y.; Visualization, J.L.; Writing—original draft, J.L. and M.T.; Writing—review and editing, M.T., J.L. and X.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This work received financial support from several sources, including the Leading Fund Project of Science and Technology Innovation of the Ningxia Academy of Agricultural and Forestry Sciences (NKYG-22-03), the Natural Science Foundation of Ningxia Hui Autonomous Region (2023AAC03426), the Chinese Academy of Sciences ‘Western Light’ Talent Training Program (‘Western Young Scholars’) Project (XAB2022YW16), the Ningxia Hui Autonomous Region key re-search and development project (2022BBF02025), and the National Watermelon Industry Technol-ogy System Project (CARS-25).

Institutional Review Board Statement

This manuscript does not contain any studies with human or animal subjects.

Data Availability Statement

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

Conflicts of Interest

The authors have declared no conflict of interest.

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Figure 1. Taxonomic composition of soil bacteria community. Operational taxonomic unit (OTU) (A) and sequence of bacteria (B) in all soil samples and relative abundance of (C) bacteria at the phylum level in soil under different concentrations of vermicompost, (n = 3).
Figure 1. Taxonomic composition of soil bacteria community. Operational taxonomic unit (OTU) (A) and sequence of bacteria (B) in all soil samples and relative abundance of (C) bacteria at the phylum level in soil under different concentrations of vermicompost, (n = 3).
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Figure 2. Taxonomic composition of soil fungal community. Operational taxonomic unit (OTU) (A) and sequence of fungi (B) in all soil samples and relative abundance of (C) fungi at the phylum level in soil under different concentrations of vermicompost, (n = 3).
Figure 2. Taxonomic composition of soil fungal community. Operational taxonomic unit (OTU) (A) and sequence of fungi (B) in all soil samples and relative abundance of (C) fungi at the phylum level in soil under different concentrations of vermicompost, (n = 3).
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Figure 3. Soil microbial community alpha diversity index. Bacterial (A,C,E,G) and fungal alpha diversity (B,D,F,H) in soil microbial community, (n = 3). Values are mean ± standard error (SEM), with bars indicating SE. Different lowercase letters mean significant difference at p < 0.05 among different concentrations of vermicompost at 0.05 level.
Figure 3. Soil microbial community alpha diversity index. Bacterial (A,C,E,G) and fungal alpha diversity (B,D,F,H) in soil microbial community, (n = 3). Values are mean ± standard error (SEM), with bars indicating SE. Different lowercase letters mean significant difference at p < 0.05 among different concentrations of vermicompost at 0.05 level.
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Figure 4. Bacteria (A) and fungi (B) of soil principal coordinate analysis (PCoA) based on Bray–Curtis dissimilarities at operational taxonomic units (OTU) level, (n = 3).
Figure 4. Bacteria (A) and fungi (B) of soil principal coordinate analysis (PCoA) based on Bray–Curtis dissimilarities at operational taxonomic units (OTU) level, (n = 3).
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Figure 5. Effect of different concentrations of vermicompost on photosynthetic index and chlorophyll content of melon leaves: (A) photosynthetic rate, (B) transpiration rate, (C) stomatal conductance, (D) intercellular carbon dioxide concentration, and (E) chlorophyll content of melon leaves. (Note: Values are mean ± standard error. F is F-value, statistical value of F-test; p value is probability greater than the calculated value; significance p ≤ 5%, 1%, and 0.1% levels, respectively. The a and b represent significant difference at p < 0.05 among corresponding water content at 0.05 level).
Figure 5. Effect of different concentrations of vermicompost on photosynthetic index and chlorophyll content of melon leaves: (A) photosynthetic rate, (B) transpiration rate, (C) stomatal conductance, (D) intercellular carbon dioxide concentration, and (E) chlorophyll content of melon leaves. (Note: Values are mean ± standard error. F is F-value, statistical value of F-test; p value is probability greater than the calculated value; significance p ≤ 5%, 1%, and 0.1% levels, respectively. The a and b represent significant difference at p < 0.05 among corresponding water content at 0.05 level).
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Figure 6. Redundancy analysis of the relative abundance of soil bacteria (A) and fungal (B) communities and soil properties and soil enzyme activity under different concentrations of vermicompost. Soil factors indicated include pH, AN (available nitrogen), OM (organic matter), AP (available phosphorus), AK (available potassium), and biomass (melon yield).
Figure 6. Redundancy analysis of the relative abundance of soil bacteria (A) and fungal (B) communities and soil properties and soil enzyme activity under different concentrations of vermicompost. Soil factors indicated include pH, AN (available nitrogen), OM (organic matter), AP (available phosphorus), AK (available potassium), and biomass (melon yield).
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Figure 7. Spearman’s correlation of advanced Cor link between bacterial (A) and fungal (B) relative abundance of soil and melon nutrition.
Figure 7. Spearman’s correlation of advanced Cor link between bacterial (A) and fungal (B) relative abundance of soil and melon nutrition.
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Table 1. Chemical properties and soil enzyme activity of soil under different concentrations of vermicompost.
Table 1. Chemical properties and soil enzyme activity of soil under different concentrations of vermicompost.
TreatmentpHAN (mg/kg)OM (g/kg)AP (mg/kg)AK (mg/kg)Biomass (kg/m2)UE (U/g)SC (U/g)CAT (U/g)POD (U/g)ALP (U/g)
control8.34 ± 0.03 a125 ± 2.0834.33 ± 0.59171.11 ± 1.59 c234.21 ± 2.76 a1847.73 ± 37.61 d1241.29 ± 28.493.57 ± 0.29 b18.4 ± 0.284.91 ± 0.83 c10,693.68 ± 327.62
T18.30 ± 0.02 a121.33 ± 1.4537.86 ± 0.28221.93 ± 2.63 a214.92 ± 1.92 b2524.89 ± 18.12 b1365.09 ± 53.24.02 ± 0.13 b18.77 ± 1.1411.5 ± 1.04 a12,365.07 ± 44.12
T28.24 ± 0.01 ab125 ± 4.0437.35 ± 1.58211.65 ± 1.88 b235.82 ± 1.00 a2882.82 ± 17.42 a1261.55 ± 26.094.81 ± 0.16 a19.16 ± 0.099.02 ± 1.15 ab11,295.23 ± 1300.06
T38.18 ± 0.06 b135 ± 5.5137.32 ± 0.68218.3 ± 2.55 ab208.38 ± 0.47 c2418.48 ± 21.39 c1319.22 ± 10.92.9 ± 0.09 c20.12 ± 0.187.75 ± 0.42 bc12,318.43 ± 551.57
FpFpFpFpFpFpFpFpFpFpFp
T4.310.042.600.133.040.092.8490.10519.2810.001294.3420.0002.8490.10519.2810.0011.5410.2779.1570.0061.2660.35
Note: Values are mean ± standard error. F is F-value, statistical value of F-test; p value is probability greater than the calculated value; significance p ≤ 5%, 1%, and 0.1% levels, respectively. The a, b and c mean significant difference at p < 0.05 among corresponding water content at 0.05 level. Soil factors indicated include AN (available nitrogen), OM (organic matter), AP (available phosphorus), AK (available potassium), Biomass (melon yield), UE (urease), SC (sucrose), CAT (catalase), POD (peroxidase), ALP (alkaline phosphatase).
Table 2. Statistical test of analysis of similarity (ANOSIM) and permutational multivariate one-way analysis of variance (PERMANOVA) of the differences in soil bacterial and fungal community compositions measured by amplicon sequencing under different concentrations of vermicompost, (n = 3).
Table 2. Statistical test of analysis of similarity (ANOSIM) and permutational multivariate one-way analysis of variance (PERMANOVA) of the differences in soil bacterial and fungal community compositions measured by amplicon sequencing under different concentrations of vermicompost, (n = 3).
TypeTreatmentdfPERMANOVAANOSIM
FpRp
BacteriaT33.1880.00010.71930.0003
FungiT325.910.00010.97840.0003
Table 3. Nutritional quality of melon under different concentrations of vermicompost. (Different lowercase letters mean significant difference at p < 0.05 among different concentrations of vermicompost at 0.05 level).
Table 3. Nutritional quality of melon under different concentrations of vermicompost. (Different lowercase letters mean significant difference at p < 0.05 among different concentrations of vermicompost at 0.05 level).
TreatmentTotal SugarCentral Soluble Solids Content (%)Vitamin CSoluble Protein ContentSoluble Carbohydrate ContentOrganic Acid
control6.4 ± 0.1 b14.3 ± 0.1 c11.0 ± 0.0 d0.3 ± 0.04.2 ± 0.0 c3.0 ± 0.3 c
T16.4 ± 0.0 b14.4 ± 0.0 c11.8 ± 0.0 c0.3 ± 0.04.5 ± 0.1 b9.0 ± 1.0 b
T26.7 ± 0.0 a16.4 ± 0.0 a13.0 ± 0.0 a0.3 ± 0.04.2 ± 0.0 c10.9 ± 0.1 a
T36.4 ± 0.1 b14.7 ± 0.0 b12.3 ± 0.1 b0.3 ± 0.04.9 ± 0.0 a9.6 ± 0.1 ab
FpFpFpFpFpFp
T6.10.0561.30.0920.10.00.50.784.60.041.90.0
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Tian, M.; Yu, R.; Guo, S.; Yang, W.; Liu, S.; Du, H.; Liang, J.; Zhang, X. Effect of Vermicompost Application on the Soil Microbial Community Structure and Fruit Quality in Melon (Cucumis melo). Agronomy 2024, 14, 2536. https://doi.org/10.3390/agronomy14112536

AMA Style

Tian M, Yu R, Guo S, Yang W, Liu S, Du H, Liang J, Zhang X. Effect of Vermicompost Application on the Soil Microbial Community Structure and Fruit Quality in Melon (Cucumis melo). Agronomy. 2024; 14(11):2536. https://doi.org/10.3390/agronomy14112536

Chicago/Turabian Style

Tian, Mei, Rong Yu, Song Guo, Wanbang Yang, Shengfeng Liu, Huiying Du, Jinjin Liang, and Xingxu Zhang. 2024. "Effect of Vermicompost Application on the Soil Microbial Community Structure and Fruit Quality in Melon (Cucumis melo)" Agronomy 14, no. 11: 2536. https://doi.org/10.3390/agronomy14112536

APA Style

Tian, M., Yu, R., Guo, S., Yang, W., Liu, S., Du, H., Liang, J., & Zhang, X. (2024). Effect of Vermicompost Application on the Soil Microbial Community Structure and Fruit Quality in Melon (Cucumis melo). Agronomy, 14(11), 2536. https://doi.org/10.3390/agronomy14112536

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