1 Introduction

Vermicompost is produced by earthworms’ digestion of organic waste (e.g., food waste, horticultural waste, poultry droppings, and food industry sludge) (Yadav and Garg 2011; Mendoza-Hernández et al. 2014; Huang et al. 2014; Lalander et al. 2015). This material has received increased attention in recent years because of its interesting physical, chemical, and biological characteristics. Vermicompost is a sustainable source of macro- and micro-nutrients (Atiyeh et al. 2000a, b), and the mineral nutrient elements in vermicompost are easily absorbed by plants (Edwards and Burrows 1988; Orozco et al. 1996; Atiyeh et al. 2000a, b). Furthermore, vermicompost has a fine granular structure with a large surface area, which allows it to absorb and retain nutrients (Zhao and Huang 1991). A large number of plant hormones are found in vermicompost (e.g., IAA, GA3, kinetin) and their presence may be the result of jointing activity of earthworms and microorganisms (Ravindran et al. 2016). Overall, vermicompost has the basic characteristics associated with a material that could be employed to improve soil quality. The application of vermicompost has been found to be an effective method for rejuvenation of soil fertility, enrichment of available nutrient pools, and conservation of water (Makode 2015). Vermicompost amendments can increase the dry mass and yield of greenhouse crops (Norman and Clive 2010; Warman and Anglopez 2010; Little et al. 2011), and significantly suppress root pests via the modulation of soil properties and plant defenses, particularly for susceptible plants (Xiao et al. 2016). The use of vermicompost as an organic fertilizer is considered a better alternative to inorganic fertilizers (Joshi et al. 2013).

Soil microorganisms play an important role in the recycling and transformation of nutrients. The sustainability of terrestrial agroecosystems is indicated by microbial diversity and activity (Su et al. 2015), and the application of both organic and inorganic fertilizers are beneficial for the stability of the original soil microorganism community structure (Ding et al. 2016). Soil fungi are important soil microorganisms, and some species promote the healthy growth of plants, whereas others can cause harm to plants. Beneficial fungi include Chaetomium globosum (Aggarwal et al. 2014), uncultured Glomus (Hassan et al. 2013), uncultured Trichoderma (Sharma et al. 2012), and Mortierella alpina (Al-Shammari et al. 2013). Harmful fungi include Fusarium oxysporum (Fravel et al. 2003), Cladosporium sp. (Papazlatani et al. 2016), Acremonium cucurbitacearum (Bruton et al. 2000), Fusarium solani (Oddino et al. 2008), Verticillium dahliae (Lopez-Escudero and Blanco-Lopez 2005), and Rhizopycnis vagum (Westphal et al. 2011). As soil fungi have a clear and direct relationship with soil quality (Gilsotres et al. 2005; Six et al. 2006), it is important to pay attention to the interactive effects of vermicompost on soil fungal communities, particularly in continuous cropping schemes in greenhouses.

Cucumber is one of main greenhouse-cultivated crops around the globe. In this study, we compared the performances of cucumber plants grown under continuous cropping on soils that had received amendments of organic fertilizer, inorganic compound fertilizer, or vermicompost as the basal fertilizer. The following characteristics were assessed: (1) cucumber fruit yield and quality under continuous cropping conditions and (2) the influence of the fertilizer amendments on soil properties under continuous cropping. We specifically focused on the influence of a vermicompost amendment on the soil fungal community, and explored the relationship of vermicompost properties and the soil fungal community. Based on the widely reported positive effects of vermicompost on crops, we hypothesized that replacement of a portion of inorganic fertilizer with vermicompost in a greenhouse would have the following consequences: (1) improved fruit yield and quality, (2) increased mineral nutrient supplies in the soil, and (3) enhanced physicochemical and microbiological properties in soil under continuous cropping conditions.

2 Materials and methods

2.1 Experimental materials and design

The following soil amendments were used in this study: inorganic compound fertilizer (N-P2O5-K2O 15-15-15) (Jiangsu Middle East Group Co., Ltd., China,), chicken manure-based organic fertilizer (Nanjing Jiahe Organic Fertilizer Co., Ltd., China), and vermicompost, a by-product of the digestion of cow manure by earthworms (Eisenia fetida) (Yangzhou Agricultural Environmental Safety Technical Service Center, Jiangsu, China). The experimental soil had a sandy loam texture, and had been used in rice cultivation prior to the experimental period. The properties of the organic fertilizer, vermicompost, and soil were determined according to Lu (2000) and are summarized in Table 1.

Table 1 The properties of organic fertilizer, vermicompost, and soil
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The experiments were conducted in greenhouses (8.0 × 50 m) at the Yangzhou University Shatou test base (32.5°N, 119.31°E), located in the Yangtze River region where modern agriculture in China was developed. In this experiment, cucumber (Cucumis sativus L.) was planted in large (60 cm) and small (30 cm) interval patterns, and plants were spaced 30 cm apart. Cucumbers were planted twice per year (i.e., April to July and September to December), and cucumber crops were continuously cultivated for 4 years (April 2012 to July 2015) in greenhouses that were constantly covered with plastic film. The soil remained fallow when cucumbers were not being cultivated. A randomized block design with three replicates was used, and 12 plots (3.0 × 9.0 m) were established. To prevent contamination, a ground separator (5 cm in height) was placed between each plot. Inorganic compound fertilizer, organic fertilizer, and vermicompost were applied as the basal fertilizer to the soil surface, and rotary tillage and ridging were then performed during the 15 days prior to the transplantation of cucumber seedlings. Based on a model of 3000 kg/ha of organic material equates to 150 kg/ha of inorganic fertilizer, the following basic fertilizer amendments were used: inorganic compound fertilizer (750 kg/ha) amendment (FT), inorganic compound fertilizer (600 kg/ha) and organic fertilizer (3000 kg/ha) amendment (FC), inorganic compound fertilizer (600 kg/ha) and vermicompost (3000 kg/ha) amendment (VP), and no basic fertilizer amendment (CK). Inorganic compound fertilizer was also applied as a topdressing (750 kg/ha) to all treatments when the cucumber plants entered the fruiting stage. The management measures employed in the greenhouse were consistent with those used in field production.

2.2 Cucumber quality and yield

During the early stage of cucumber seedling growth, six plants were selected from each plot, and the yield per plant was determined by measuring the weight of each plant during the 2012–2015 spring seasons (April to July). Samples were collected to determine the quality of cucumber fruit before the topdressing application. The quality of cucumber fruits was measured in June of 2015. The nitrate content of the fruit was extracted using boiling water and determined by UV spectrophotometry (Qi 2003). The soluble solid content was measured using an Abbe refractometer (2WA-G, Shanghai Fifth Optical Instrument Factory, China), soluble protein content was determined using Coomassie brilliant blue G-250 staining, soluble sugar content was measured using the anthrone colorimetric method, organic acid content was determined by the NaOH direct titration method, and vitamin C content was measured using a titration method with 2,6-dichlorophenol (Qi 2003). The sugar-acid ratio of fruit was calculated as the ratio of soluble sugar to organic acid contents.

2.3 Basic soil and nutrient properties

Soil samples were collected at a depth of 0–15 cm before the annual topdressing application in June of each year. Each sample was divided into two parts, one part was directly used for the determination of soil microbial nitrogen (MBN) and soluble organic carbon (DOC) and the second part was air-dried and used for the determination of other variables. The pH and electrical conductivity (EC) were measured from 2012 to 2015, but other variables were only measured in 2015. The methods described by Lu (2000) were used to estimate soil properties. A soil suspension was prepared at a 1:5 ratio of soil-to-water (m:v) using double-distilled water and used to measure pH (PXSJ-216F, Rex, China) and EC (DDSJ-308F, Rex, China). The amount of total nitrogen (TN) in the soil was determined by distillation titration, the ammonia nitrogen (NH4 +-N) content was measured using indophenol blue spectrophotometry, and the nitrate nitrogen (NO3 −-N) content was estimated using an ultraviolet spectrophotometer. Soil samples were fumigated with chloroform and mixed with K2SO4 solution, and the resulting alkali distillation liquid was then used to determine MBN. The organic matter (OM) content was determined using a K2Cr2O7-H2SO4 solution and external heating method. A clarification solution was prepared after extraction using a 1:5 ratio of soil-to-water (m:v) in double-distilled water, and this was used to measure the DOC using a total organic carbon analyzer (TOC-L, Shimadzu, Japan). Total phosphorus (TP) was obtained via HClO4-H2SO4 digestion and then molybdenum blue colorimetry. Determination of the available phosphorus (Olsen-P) was performed using NaHCO3 solution extraction and molybdenum blue colorimetry. The available potassium (AK) was measured using ammonium acetate solution extraction and a flame photometric method. Soil bulk density was determined using a cutting ring, and the soil water content was measured by drying the soil at 80 °C.

2.4 Soil microbial properties

Rhizosphere soil samples were collected in June 2015 to determine the diversity of soil fungal communities; the samples were obtained as described by Ling et al. (2014). All samples were processed individually, and genomic DNAs present in each composite sample were extracted using a FastDNA® SPIN Kit for soil (MP Biomedicals, USA) according to the manufacturer’s instructions. Three replicate DNA extractions were conducted for each soil sample. The composition of the fungal community in each soil sample was determined using Illumina Miseq sequencing, as described by Magoč and Salzberg (2011). The protocol for sequencing the samples was as follows: (1) PCR was used to amplify the internal transcribed spacer (ITS) ITS1 region using ITS1F (5′-CTTGGTCATTTAGAGGAAGTAA-3′) and ITS2 (5′-GCTGCGTTCTTCATCGATGC-3′) primers, (2) Illumina sequencing libraries were prepared using PCR products as templates, and (3) Illumina Miseq system was used to sequence the ITS1 region.

Filtering and connection of the original double-terminal sequences were then conducted. Firstly, the FASTQ sequences (raw data obtained by Illumina Miseq sequencing) of two ends were filtered based on the weight of the fragment using a sliding window approach with a 5-bp window size and a 1-bp step. The sliding window began at the first base position, and the average weight of base was calculated based on the Q20 score (i.e., base accuracy ≥99%). The sequence was truncated when bases lower than Q20 were detected, and the final sequence length was restricted to >150 bp (sequences with ambiguous base calls (N) were excluded). Secondly, sequences were connected with FLASH software (Lievens et al. 2007) using an overlap of >10 bp between reads 1 and 2, and base mismatches were not allowed. Lastly, the effective sequence of each sample (with fully matched indices) was extracted based on the sequence information used to distinguish the samples.

2.4.1 Quality sequence filtering

Quality sequences were filtered using Qiime software (version 1.9.0) (Caporaso et al. 2010; Scarlett et al. 2013), and the uchime method found in the mothur software package (version 1.31.2; http://www.mothur.org/) was used to remove chimeric sequences (Schloss et al. 2009; Edgar et al. 2011). Erroneous sequences were removed, including sequences with 5′ prime mismatched bases greater than 1, sequences containing ambiguous base calls (N), sequences containing more than 8 contiguous bases, sequences less than 150 bp in length, and chimeric sequences.

2.4.2 Clustering and annotation of operational taxonomic units

The uclust method found in the Qiime software package was used to cluster the high-quality sequences, and a 97% sequence similarity criterion was used to assess sequence clusters (Edgar et al. 2011). The longest sequence of each class was selected as the representative sequence. A BLAST search (Altschul et al. 1990) based on the Qiime software package was used to compare the sequences to those in sequence databases, and taxonomic information on each operational taxonomic unit (OTU) sequence was obtained (Altschul et al. 1990). The FastTree program (Price et al. 2009) was used to construct a phylogeny based on the representative OTU sequences. In order to ensure the accuracy of the results, OTUs with an abundance value <0.001% of the total number of sequences were removed (Bokulich et al. 2012). The ACE index was used to measure community richness (Pitta et al. 2010), and the Shannon index was used to evaluate microbial diversity in soil samples (Shannon and Weaver 1949).

2.5 Statistical analysis

The data (n = 3) were subjected to one-way analysis of variance (ANOVA) and multivariate analysis of variance (MANOVA) using the SPSS software package for Windows (SPSS, version 18.0, Chicago, USA). When statistical significance (p < 0.05) was detected, the mean values subjected to Duncan’s multiple range tests. Pearson’s two-tailed tests were performed to establish correlations between soil physical and chemical properties and cucumber development (n = 3). A principal component analysis (PCA) was used to analyze the characteristics of the soil fungal community. The relationship between soil environmental factors and soil fungal community composition was analyzed using a redundancy analysis (RDA).

3 Results

3.1 Cucumber yield and quality

Fruit yields in the greenhouse fell with continuous cropping (Table 2). This effect presented in all treatments over the experimental period, 2012 to 2015. The highest yield (1.53 kg/plant) was obtained in 2012 from plants in the vermicompost plus inorganic compound fertilizer treatment, and yields in the other treatments were followed in the following sequence: organic fertilizer plus inorganic compound fertilizer, inorganic compound fertilizer amendment, and control (no amendment). After 4 years of continuous cropping, the yield in the VP treatment declined by 19.4%, yields in the FC, FT, and CK treatments declined by 41.0, 30.9, and 22.2%, respectively. Basal fertilizer amendment clearly increased the yield of cucumber fruit regardless of whether organic or inorganic fertilizers were used; the VP treatment appeared to be best at maintaining fruit yield under continuous cropping in a greenhouse than the FC and FT treatments.

Table 2 Characteristics of the cucumber fruit yield and the soil pH and EC in different base fertilizer treatments from spring of 2012 to 2015
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Application of a basal fertilizer significantly increased cucumber fruit quality (Table 3). Compared to the CK treatment, VP treatment significantly increased soluble solids, soluble sugar, vitamin C, and soluble protein contents as well as the sugar-acid ratio of cucumber fruits after 4 years of continuous cropping (in 2015). Some quality indices of FT were significantly higher than those of the CK treatment, including vitamin C content, nitrate content, and the sugar-acid ratio. The level of nitrates in the fruit from the FT treatment was 3.5-fold higher than in the CK treatment. Nitrate contents of fruit from the FC treatment were significantly higher than those in the CK treatment, but were significantly lower than those of the FT treatment. Overall, the VP treatment was the best at maintaining the quality of the fruit after 4 years of continuous cropping.

Table 3 Cucumber fruit qualities, and soil nitrogen, carbon, phosphorus, potassium, water content, and bulk density in the four different base fertilizer treatments in spring of 2015
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3.2 Characteristics of soil properties

3.2.1 Characteristics of soil basic physical and chemical properties

Both continuous cropping of cucumbers and basal fertilizer amendments under greenhouse conditions resulted in a gradual decrease in soil pH and a gradual increase in soil electrical conductivity (EC) (Table 2). After 4 years of continuous cropping, the use of basal fertilizer amendments had decreased soil bulk density and increased soil water content (Table 3). Soil pH in the CK treatment was significantly higher than that of VP-treated soil in the spring seasons of 2014 and 2015, and was also significantly higher than those of the FT and FC treatments in 2015. The pH of VP-treated soil (6.39) was significantly lower than that of the other treatments in 2015. The EC of FC-treated soil (0.41 mS/cm) in spring 2012 was significantly higher than those of the other treatments, while the EC of soil in the CK treatment (0.82 mS/cm) in spring 2013 was significantly lower than those of the other treatments. Moreover, the EC of FT-treated soil (2.76 mS/cm) was significantly higher than those of the other treatments in 2015. The soil bulk density values of VP-treated soil were significantly lower than those of the CK treatment, while the soil water content was significantly greater than that of the CK treatment in 2015. The soil water content of FC-treated soil was significantly lower than that in the VP treatment in 2015. The various analyses indicated that the VP treatment led to the largest decline in soil pH and soil bulk density and the largest increase in soil water content after 4 years of continuous cropping. The FT treatment caused the largest increase in soil EC.

3.2.2 Characteristics of carbon, nitrogen, phosphorus, and potassium in soil

In the three treatments in which basal fertilizer was applied, soil nitrogen characteristics were significantly different at the end of the experiment compared to the control (Table 3). TN content was highest in the FT treatment, NH4 +-N content was highest in the CK treatment, and microbial nitrogen (MBN) content was highest in the VP treatment. Nitrate nitrogen (NO3 −-N) content in the CK treatment was significantly lower than those of the FC, FT, and VP treatments, and the differences in TN, NH4 +-N, NO3 −-N, and MBN between FT and FC treatments were not significant in 2015. The TN (1.95 g/kg) and NH4 +-N (4.48 mg/kg) contents in the FT treatment were significantly larger than those in the VP treatment, but the MBN (125.25 mg/kg) content in the VP treatment was significantly larger than that in the FT treatment. In comparison to the CK treatment, the FT and FC treatments increased in TN and NO3 −-N contents, and caused reductions in soil NH4 +-N content. Furthermore, the VP treatment increased soil NO3 −-N and MBN and reduced soil NH4 +-N content.

Basal fertilizer amendments also significantly influenced soil carbon, phosphorus, and potassium contents (Table 3). Soil organic matter (OM), soluble organic carbon (DOC), total phosphorus (TP), available phosphorus (Olsen-P), and available potassium (AK) contents were significantly lower in 2015 in the CK treatment than in treatments given basal fertilizer amendments. In the FC treatment, soil OM was significantly higher than in the VP and FT treatments, but there were no significant differences in soil DOC contents among the FC, VP, and FT treatments. Soil TP and AP contents in the VP treatment were significantly higher than those of the FT and FC treatments, while the soil AK content of the FT treatment was significantly higher than those of the VP and FC treatments. These results indicate that the application of organic fertilizer promoted the accumulation of soil OM and that basal fertilizer amendments had no significant effects on soil DOC contents. The VP amendment increased TP and AP accumulation, and the FT amendment increased soil AK.

3.3 Relationship between cucumber yield and quality and soil properties

Cucumber fruit yield and quality were significantly affected by soil properties. Thus, the increases in soil water, TP, AP, and MBN contents were positively correlated with cucumber yield (Table 4). However, soil TN, NH4 +-N, pH, and bulk density had a significant negative correlation with cucumber yield. The NO3 −-N, MBN, DOC, TP, Olsen-P, and soil water contents had a positive correlation with cucumber fruit quality, but the soil TN, NH4 +-N, pH, and bulk density had a significant negative opposite correlation. Soil OM content had a significant positive correlation with the nitrate content of the fruit, and soil EC had a positive correlation with the sugar-acid ratio of the fruit. The soil AK content was significantly and positively correlated with vitamin C content, sugar-acid ratio, and nitrate content of fruit, but was significantly and negatively correlated with organic acid content.

Table 4 Correlation analysis of soil physical and chemical properties with development of cucumber
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3.4 Characteristics of soil fungi

3.4.1 Structure of the soil fungal community

The number of reads sequenced from soil samples ranged from 97,589 (FT treatment) to 86,476 (VP treatment), and the proportion of high-quality reads ranged from 75.7% (FT treatment) to 74.9% (VP treatment) (Table 5). The lengths of the high-quality sequences were in the range of 240–270 bp. In total, 687 OTUs were identified from rhizosphere soil from all treatments; 359 common OTUs were identified (data not shown).

Table 5 Summary of pyrosequencing data and diversity estimates for the rhizosphere soil of different base fertilizer treatments in spring of 2015
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Application of basal fertilizer significantly affected the structure of the soil fungal community. The VP treatment increased soil fungal diversity (Shannon index) and richness (ACE index) compared to the other treatments (Table 5). A principal component analysis (PCA) indicated that the differences in the fungal community structure between FT and CK treatments were small. However, fungal community structures in the FC and VP treatments differed from that in the CK treatment, and these differences were especially prominent after the VP treatment (Fig. 1).

Fig. 1
figure 1

Principal component analysis (PCA) for the rhizosphere soil of different base fertilizer treatments in spring of 2015. CK control, no fertilizer addition; FT inorganic fertilizer; FC organic fertilizer/inorganic fertilizer mixture; VP vermicompost/inorganic fertilizer mixture (see Sect. 2 for the description of the mixtures)

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The soil fungal community was dominated by the Ascomycota (55.9%), and other phyla were present at much lower levels, e.g., Basidiomycota (5.7%), Zygomycota (4.2%), Chytridiomycota (0.7%), and Glomeromycota (0.3%) (Fig. 2a). Compared with the CK treatment, the relative abundance of Ascomycota and Chytridiomycota increased significantly in the VP treatment, while the Glomeromycota and Zygomycota were significantly decreased. In the FC treatment, the relative abundance of Ascomycota, Glomeromycota, and Zygomycota decreased significantly. In the FT treatment, the relative abundance of Chytridiomycota significantly increased but that of Glomeromycota and Zygomycota decreased. The relative abundance of Basidiomycota decreased significantly in the VP, FC, and FT treatments.

Fig. 2
figure 2

The distribution of soil fungal species (phylum and class) in different base fertilizer treatments in spring of 2015. CK control, no fertilizer addition; FT inorganic fertilizer; FC organic fertilizer/inorganic fertilizer mixture; VP vermicompost/inorganic fertilizer mixture (see Sect. 2 for the description of the mixtures)

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At the class level, Sordariomycetes (40.3%) predominated over Dothideomycetes (4.2%), Eurotiomycetes (3.2%), Agaricomycetes (3.0%), and Tremellomycetes (2.7%) in rhizosphere soil (Fig. 2b). The relative abundance of Dothideomycetes was significantly higher in the CK treatment than in fertilizer-amended soils. The relative abundance of Eurotiomycetes and Sordariomycetes in the VP treatment and of Agaricomycetes and Tremellomycetes in the CK treatment was higher than in the other treatments.

3.4.2 Beneficial and harmful fungi

Next, we examined the relative abundance of harmful fungi in soils from the different treatments. The relative abundance of F. solani and R. vagum in the CK treatment was significantly higher than in the other treatments; Cladosporium sp. were significantly more abundant in the FT treatment. The relative abundance of F. oxysporum in the CK and FT treatments was significantly greater than that in the FC and VP treatments (Fig. 3a). In the FT treatment, a decrease in the relative abundance of F. solani was observed. In the FC and VP treatments, a reduction in the relative abundance of F. solani, F. oxysporum, Cladosporium sp., and R. vagum was found. Overall, the application of basal fertilizers to the soil decreased the relative abundance of harmful fungi. The organic fertilizers had a significantly greater effect on the reduction of harmful fungi than the inorganic fertilizer; the beneficial effects of VP were especially pronounced. Application of basal fertilizers also significantly changed the relative abundance of beneficial soil fungi. The relative abundance of M. alpina and C. globosum were significantly higher in the CK treatment than in fertilizer-treated soil. The relative abundance of uncultured Trichoderma was significantly greater in the FT treatment than that in other treatments (Fig. 3b). In general, fertilization treatments decreased the abundance of beneficial fungi in the soil. In the FC treatment, the abundance of M. alpina was significantly decreased compared to the VP treatment, although the abundance of uncultured Trichoderma was greater in the FC treatment.

Fig. 3
figure 3

The relative abundance of soil pathogenic fungi and soil beneficial fungi for the rhizosphere soil of different base fertilizer treatments in spring of 2015. CK control, no fertilizer addition; FT inorganic fertilizer; FC organic fertilizer/inorganic fertilizer mixture; VP vermicompost/inorganic fertilizer mixture (see Sect. 2 for the description of the mixtures). Mean values ± standard error (n = 3) are shown; means shared with a common letter in the same column indicate no significant differences between treatments (p < 0.05) based on Duncan’s multiple range test

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3.5 Relationship of soil fungal community and soil properties

Redundancy analysis (RDA) indicated that soil environmental factors altered the composition of soil fungal communities (Fig. 4). The first two RDA axes explained 88.77% of the cumulative variance of the fungi-environment relationship, suggesting a strong relationship between the composition of the fungal community and environmental variables. Since the scaling is focused on inter-sample distances, we can independently interpret each arrow as pointing in the direction in which the sample scores would shift with an increase in the value of that environmental variable. The length of the arrow allows us to compare the size of such an effect across the environmental variables, and the angle between the arrows and axes of the environmental variables can be used to approximate their correlations. The first RDA axis explained 68.54% of the cumulative variance; therefore, environmental variables such as soil water, MBN, TP, pH, and NH4 +-N contents play important roles in fungal community composition (p < 0.05), based on their relatively greater lengths and smaller angles relative to the first axis.

Fig. 4
figure 4

Redundancy analysis (RDA) of the fungi community for the rhizosphere soil of different base fertilizer treatments in spring of 2015. CK control, no fertilizer addition; FT inorganic fertilizer; FC organic fertilizer/inorganic fertilizer mixture; VP vermicompost/inorganic fertilizer mixture (see Sect. 2 for the description of the mixtures); S1 Fusarium solani; S2 Fusarium oxysporum; S3 Acremonium sp.; S4 Humicola nigrescens; S5 Cladosporium sp.; S6 Rhizopycnis vagum; S7 Fusarium oxysporum; S8 Mortierella alpina; S9 Chaetomium globosum; S10 uncultured Trichoderma; S11 Fusarium nematophilum; S12 Alternaria destruens; S13 Ascomycota sp.; S14 Emericellopsis sp.; S15 Hypoxylon ticinense; S16 Mrakia robertii; S17 uncultured Sordariales; S18 Aspergillus ochraceus; S19 uncultured Hydnum; S20 Trichosporon asahii; S21 Aspergillus flavus; TN total nitrogen; AN ammonium nitrogen; NI nitrate nitrogen; MBN microbial nitrogen; OM organic matter; DOC soluble organic carbon; TP total phosphorus; AP available phosphorus (Olsen-P); AK available potassium; SW soil water content; BD soil bulk density

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In the ordination diagrams, pH and NH4 +-N generally showed the strongest positive correlations with the first axis, while soil water, MBN, and TP showed the strongest negative correlations. The results agreed with those of the correlation analysis between yield and environmental variables (Table 4), indicating the presence of intrinsic connections among soil properties, fungal community composition, and cucumber development.

If we project the sample point perpendicular to the arrow of a species, we obtain an approximate ordering of the values of this species across the projected samples. In the ordination diagrams, it can be seen that ordering the positions of the values for harmful fungi (e.g., F. solani, F. oxysporum, Acremonium sp., Humicola nigrescens, and Cladosporium sp.) place the VP treatment at the lowest position, suggesting that vermicompost amendment decreased the abundance of harmful fungi. Compared to the control, the abundance of beneficial fungi in the vermicompost treatment also exhibited a downward trend, but their abundance was higher than that of the other fertilizer application treatments. A sharp decrease in harmful fungi and the presence of relatively abundant beneficial fungi in the soil shows that vermicompost amendment had a positive effect on the development of healthy soil microbiota.

4 Discussion

4.1 Yield and quality responses to soil vermicompost amendment

Fertilization increases crop yield, and the beneficial effects of VP amendments are more obvious than other treatments (Yang et al. 2015). Similar results were obtained in our study in that the fertilizer amendment increased the yield of cucumber fruit even though the yield decreased yearly under continuous cropping conditions. Providing timely and adequate supplies of mineral nutrients for cucumber growth is part of the mechanism that improves yield. The use of the VP amendment aided cucumber fruit yield under continuous cropping conditions. This outcome might result from the excellent physical characteristics and abundant nutrients of VP (Zhao et al. 2010a, b; Ravindran et al. 2016) and the ability of VP to effectively regulate soil properties (Oo et al. 2015).

Nitrate content is used to evaluate the safety of vegetables, and a negative correlation exists between nitrate content and the nutritional quality of vegetables. Moreover, nitrate, amino acids, proteins, sugars, organic acids, mineral, and vitamins are closely interrelated (Blom-Zandstra 1989; Huang et al. 2011). Our previous study suggested that the overall quality of cucumbers was improved by applying VP and VP-inorganic mixed fertilizer under greenhouse conditions (Zhao et al. 2010a, b). The difference between the nitrate contents of cucumber fruits was not significant between VP amendment and lack of fertilizer amendment, despite the fact that the VP application provided a large number of mineral nutrients. Soil properties, especially biological properties, are altered by BP treatment, which also improves the development of the cucumber plants. These may be the main mechanisms that underlie the improvement of cucumber fruit quality. Vitamin C is known to have marked nucleophilic properties and the ability to capture and deactivate free radicals or reactive oxygen species produced by metals (Jiraungkoorskul and Sahaphong 2007). The application of inorganic compound fertilizers and VP has been shown to significantly increase vitamin C in fruit, but organic fertilizer amendments do not have this effect. Vitamin C content in fruit is related to the supply of mineral nutrients, and the uptake of mineral nutrients by plants depends on soil characteristics, such as cation exchange capacity, pH, microorganisms, and metal ions (Fernandes and Henriques 1991). Therefore, the vitamin C content of cucumber fruits might depend on the combined effects of soil mineral nutrients, soil properties, plant responses, and fertilizer properties.

4.2 Effects of vermicompost application on soil properties

In the present study, we found that the continuous cropping of cucumbers in a greenhouse setting resulted in decreased soil pH and increased EC, and these outcomes are consistent with previous studies. The changes result from the addition of a large number of base cations to the soil at the time of fertilization (Orozco et al. 1996; Atiyeh et al. 2000a, 2000b) and to the fact that crops selectively absorb ions, such as hydrogen ions. After seven cucumber crops, the application of VP amendment resulted in decreased soil pH that differed from those after FT and FC amendments. However, there were no significant differences detected between the EC after FC and VP treatments. The cause of this effect might be the ability of VP to promote crop system development more effectively than other fertilizers and the capacity to absorb more mineral ions while simultaneously producing hydrogen ions (Edwards and Burrows 1988; Orozco et al. 1996). The unique characteristics of VP and the beneficial interaction between VP and soil (Ngo et al. 2012; Oo et al. 2015) suggest that VP amendments could significantly increase soil water-holding capacity and lower bulk density, which is conducive to the healthy growth of crops.

The nitrogen characteristics of soil directly reflect its fertility, and influence the absorption and utilization of mineral elements by plants. The addition of VP has been shown to significantly increase soil mineral nutrition (e.g., NH4 +-N, NO3 −-N, and phosphorus), decrease soil organic matter content, and influence the rates of nutrient cycling (Arancon et al. 2006; Yang et al. 2015). Our results here showed that application of fertilizer resulted in the accumulation of NO3 −-N in the soil. The microbial nitrogen (MBN) content of VP was also significantly higher than those of the other treatments.

We observed a decrease in the carbon and nitrogen contents in soils amended with fertilizer, and the VP amendment did not alter organic carbon content. However, compost amendment has been shown to increase soil organic carbon content compared to initial soil properties (Ngo et al. 2012). Our data indicated that the soil organic matter (OM) and soluble organic carbon (DOC) contents increased significantly following application of fertilizer over a 4-year period; these results are consistent with previous studies that showed increased carbon storage by exogenous organic amendments in addition to improvements in several soil functions related to the presence of organic matter (Lashermes et al. 2009; Ngo et al. 2012). In the present study, the FT and VP treatments were more conducive to soil carbon conversion and the enhancement of soil microbial activity, because the soil microbes could use DOC more efficiently. Soil available-N and AP were increased by VP treatment, and the integration of bioorganic nutrient supplements significantly maintained soil health and productivity on a long-term basis for sustainable crop production (Yadav et al. 2016). Our data demonstrated that an integrated nutrient management scheme for chemical fertilizers and organic manures might offer a feasible and environmentally friendly option for soil conservation (Singh et al. 2016).

4.3 Effect of vermicompost application on soil fungus characteristics

Environmental variables play an important role in soil microbial flora divergence (Rodrigues et al. 2014); thus, soil pH and contents of NH4 +-N, NO3 −-N, Ca, and total carbon influence the characteristics of the soil microbiota (Ligi et al. 2014). It has been shown that crop growth can increase microbial nutrient mobilization capacity and alter the distribution of the soil microbial population (Marschner et al. 2011). Our results indicated that the soil fungal community after VP amendment exhibited greater differentiation than those associated with the FC and FT amendments. In soil amended with the VP treatment, MBN and TP were significantly and positively correlated with the soil fungal communities; this result is consistent with previous reports (Liu et al. 2014; Ligi et al. 2014).

Applied organic and chemical fertilizers can greatly alter the soil microorganism population (Cai et al. 2003), and an increased microbial population and their related activities in VP amended soil are key factors that influence plant resistance or tolerance to crop pathogens and nematode attacks (Arancon et al. 2006). In this study, the effect of FC treatment on the reduction of harmful fungi was significantly better than that of the FT treatment, and the beneficial effects of VP were more prominent.

Application of a suitable amount of VP might inhibit soil pests and soil-borne diseases (Edwards and Norman 2004), and might significantly decrease the number of plant parasitic nematodes and infection rates in plants (Arancon et al. 2002). Additionally, VP treatment might suppress diseases such as phytophthora, fusarium, and plasmodiophora in tomatoes (Chaoui et al. 2002). Clearly, the excellent biological properties of VP, which contains biologically active substances and large amount of functional microorganisms, are another major mechanism responsible for its beneficial effects (Tomati et al. 1987; Grappelli et al. 1987).

5 Conclusions

Continuous cropping over 4 years resulted in a decreased yield of cucumber fruit in a greenhouse, and the application of a basal fertilizer mitigated this decline in output. Moreover, basal fertilizer amendments decreased the levels of beneficial and pathogenic fungi in the soil, although VP amendment had a positive effect on the composition of a healthy soil fungal community. The use of VP amendment as the basal fertilizer significantly improved the basic soil physicochemical properties, mineral nutrient, and biological properties, and it also increased cucumber yield, and improved fruit quality. Future research will focus on the effects of VP amendment on soil bacterial community structure in a continuous cropping system.