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Article

Nitrogen Reduction with Bio-Organic Fertilizer Altered Soil Microorganisms, Improved Yield and Quality of Non-Heading Chinese Cabbage (Brassica campestris ssp. chinensis Makino)

by
Yingbin Qi
1,
Zhen Wu
1,
Rong Zhou
1,2,
Xilin Hou
3,
Lu Yu
1,
Yuxin Cao
1 and
Fangling Jiang
1,*
1
Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
2
Department of Food Science, Aarhus University, 8200 Aarhus, Denmark
3
State Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(6), 1437; https://doi.org/10.3390/agronomy12061437
Submission received: 11 May 2022 / Revised: 12 June 2022 / Accepted: 13 June 2022 / Published: 16 June 2022
(This article belongs to the Special Issue Horticultural Plants Breeding for Abiotic Stress Tolerance)
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Abstract

:
Excessively using fertilizers poses serious problems such as environmental pollution, soil degeneration, and quality and yield reduction of vegetables. This study aimed to illustrate the effect of different organic manure and inorganic fertilizers on the characteristics of soil, and the growth, yield, and quality of non-heading Chinese cabbage. There were 28 treatments in the first experiment: no fertilization (CK), conventional fertilization (100% nitrogen T1), 20% reduction of total nitrogen (T2), 30% reduction of total nitrogen (T3), and 20% or 30% reduction of total nitrogen with four kinds of fertilizers and three kinds of dosages (24 treatments). Six treatments, being selected from the first experiment based on growth of plants, were further applied to the second experiment. The results of the second experiment showed that the pH, nitrate nitrogen, and organic matter content of soil treated by N2 (20% reduction of total nitrogen with 1500 kg·ha−1 No.1: Bacillus-enriched bio-organic fertilizer) were significantly enhanced compared with T1 (100% nitrogen). The N2-treated plants showed an 11.66% increase in root activity, 9.24% enhancement in yield, 5.79% increase in vitamin C (VC), and 47.87% decrease in nitrate content compared with T1. Nitrogen reduction with bio-organic fertilizer significantly increased the dominant phyla of Gemmatimonadetes and Chytridiomycota and significantly decreased Ascomycota, and increased the dominant genera of Gemmatimonas and Bacillus and decreased Fusarium, indicating that this treatment altered the microbial community composition of soil. Redundancy analysis (RDA) showed that AP (available phosphorus), OM (organic matter), and UREA (urease activity) of the soil were significantly correlated with microbial community structure. Yield was significantly, positively correlated with Rhodanobacter and Olpidium. In conclusion, nitrogen reduction with bio-organic fertilizer benefited growth, yield, and quality of non-heading Chinese cabbage by improving the soil quality.

1. Introduction

The mineral fertilizer used in vegetable production is 2.3 times more than that used on other crops in China [1]. Consumption of fertilizer in China is about 7.73 times more than the amount in Europe, and the utilization rate of nitrogen fertilizer is only 30–40% that of the Europeans [2]. The excessive application of mineral fertilizer leads to decreased soil quality and reduced food quality, and particularly, increased nitrate accumulation in vegetal products [3]. In addition, the excessive application of chemical fertilizer also has an adverse impact on the environment [4].
Rational fertilization is crucial to promote beneficial rhizosphere interactions for sustainable agricultural production [5]. Organic fertilizer replaces parts of mineral fertilizer and can enhance the healthy development of the vegetable industry [6]. Researchers suggest that biofertilizer with mineral fertilizer is a promising approach to maintaining the soil microbiota balance by ameliorating soil pH, TN (total nitrogen content), and organic matter statuses [7]. Furthermore, bio-organic fertilizers usually contain a unique microbial community, which can activate soil, increase soil biodiversity, and improve soil enzyme activities [8,9]. Soil microorganisms have crucial roles in nutrient cycling and the fertility maintenance of soil. The soil microbiome has both direct and indirect effects on the health of plants and animals in terrestrial ecosystems [10]. Bacillus and Trichoderma are reported as well-known PGPR (plant growth-promoting rhizobacteria) which could improve the growth of plants and the resistance to diverse environmental stress [11,12,13,14]. Research showed that bio-organic fertilizer could enhance tomato yield and quality more than PGPR or organic fertilizer solely [3]. Gao et al. [15] found that six years of continuous biochar and biochar-based fertilizer application could increase Acidobacteria in peanut soil. Fulvic acid organic fertilizer could increase the quality of tomatoes [16].
Non-heading Chinese cabbage accounts for 30–40% of the vegetable multiple cropping area in the south of China [17]. The cultivated area in China increased from 533,300 ha in 2005 to 1,333,300 ha in 2020 [18]. Excessive nitrogen fertilizer application is an extremely common problem during cabbage production. The aim is to study the effects of reduced nitrogen with different commercial bio-organic fertilizers on the microbial community structure and soil characteristics, as well as on plant growth, yield, and quality, of non-heading Chinese cabbage. Our study can provide a theoretical support for scientific fertilization during crop production.

2. Materials and Methods

2.1. Materials

The seeds of non-heading Chinese cabbage “Siyuebai” and “Jinpin28” were provided by the key Chinese Cabbage Breeding Laboratory of Nanjing Agricultural University. Field experiments were conducted 2018–2019 at the Agricultural Expo Garden, Jurong, Jiangsu, China (32° N, 119°12′ E). The soil texture (0–15 cm) had a pH of 4.83, an organic matter content of 29.18 g·kg−1, a total nitrogen content of 1.50 g·kg−1, and an available potassium content of 190.00 mg·kg−1.
Mineral fertilizers (46% urea, 12% superphosphate, and 52% anhydrous potassium sulfate) were provided by Yuntianhua Co., LTD, Kunming, China. A bio-organic fertilizer named “No.1” (Bacillus 2 × 108·g−1 living bacteria count, 3-5-0.7 N-P-K) was bought from Lianye Biotechnology Co., LTD, Jiangyin, China. “Bamboo charcoal” (biochar-based fertilizer, 3-5-0.7 N-P-K) was bought from Shike Bamboo Charcoal Co., LTD, Shanghai, China. “Jiajiapei” (Trichoderma, etc., 2-2-1 N-P-K) was bought from Delong Biotechnology Co., LTD, Xi’an, China. “Fulvic acid” (3-3-1 N-P-K) was bought from Yimutian Biotechnology Co., LTD, Qingzhou, China.

2.2. Experiment Design

There were 28 treatments in the first experiment (“Siyuebai”): no fertilization (CK), conventional fertilization (the average level of fertilization that farmers commonly use, (T1), 193.2 kg·ha−1 N, 135 kg·ha−1 P2O5, 135 kg·ha−1 K2O), a 20% reduction of total nitrogen (T2), a 30% reduction of total nitrogen (T3), and a 20% or 30% reduction of total nitrogen with four bio-organic fertilizers and three kinds of dosages each. The fertilization information of each treatment is shown in Table S1. The first experiment was conducted from September to December 2018. Every treatment was set up with three repetitions in a random block arrangement. Each plot’s area was 4 m × 1.5 m with 96 plants in each repetition. All the fertilizers were applied as base fertilizer.
According to the results of the first experiment, we screened out six treatments to further initiate the second experiment (“Jinpin28”). The treatments are shown in Table 1. The second experiment was carried out from March to May 2019.

2.3. Determination Index and Method

2.3.1. Determination of Soil Characteristics

Soil samples were collected from 5 to 10 cm soil layers around the plant root and passed through a sterilized 2 mm sieve to remove rocks, roots, and organic residues. Fresh soil was stored at 4 °C for soil enzyme activity analyses and at −80 °C for DNA sequencing. The electrical conductivity (EC) and pH of soil were determined by mixing soil with deionized water at 1:2.5 and 1:5 (w/v), respectively. Nitrate nitrogen content of the soil was determined by using a continuous flow analyzer (BRAN + LUEBBE Auto Analyzer3, Hamburg, Germany) [19]. Soil organic matter and total nitrogen content were determined using an elemental analyzer (Vario EL elemental analyzer, Hanau, Germany) [20]. Available P and available K content in soil were detected using the methods of Bao [21]. The content of P, K, Ca, and Zn elements of soil and plant was determined using inductively coupled plasma mass spectrometry (ICP-MS, Agilent 7800, Santa Clara, CA, USA) [22]. Activity of soil urease and invertase was determined according to the method descried by Sun et al. [23]. Phosphatase and FDA (fluorescein diacetate) were measured following the methods of Guan [24] and Taylor et al. [25], respectively.

2.3.2. DNA Extraction and PCR Amplification

Soil subsamples for molecular analysis were kept in a freezer at −80 °C before use. Total DNA was extracted from 18 samples using the E.Z.N.A.® soil DNA Kit (Omega Bio-tek, Norcross, GA, USA) according to the manufacturer’s instructions. The DNA extract was checked on 1% agarose gel, and DNA quantity and quality were determined by the NanoDrop 2000 UV-Vis Spectrophotometer (Thermo Scientific, Wilmington, NC, USA). Three commonly used primer sets were used to study soil bacterial 16S rRNA genes and fungal 18S rRNA genes [26,27]. The PCR conditions for each primer set are shown in Table S2. The system included 0.4 μL of TransStart FastPfu DNA Polymerase and 10 ng of template DNA with ddH2O up to 20 μL. PCR reactions were performed in triplicate according to the manufacturer’s instructions and quantified by using the Quantus™ Fluorometer (Promega, Madison, WI, USA). The PCR product was extracted from 2% agarose gels and purified with the AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA, USA). Purified amplicons were pooled in equimolar and then sent for paired-end sequencing on an Illumina MiSeq PE 300 × 2 Sequencer (Majorbio Bio-Pharm Technology Co., Ltd., Shanghai, China).

2.3.3. Growth, Yield, Quality, and Photosynthetic Parameter Indexes

Photosynthesis was determined with the Li-6400 (LI-COR Inc. Lincoln, NE, USA) from 9–11 a.m. Chlorophyll content was determined with the ethanol (95%) extraction-colorimetric method [28]. Root vitality, nitrate content, soluble protein content, VC (L-ascorbic acid, AsA) content, and total soluble sugar content were determined using TTC (triphenyltetrazolium chloride) [29], salicylic acid colorimetry [30], Coomassie Brilliant Blue G-250 colorimetry, o-phenanthroline colorimetry [31], and anthrone colorimetry [32], respectively.

2.4. Statistical Analysis

Alpha-diversity characteristics in each soil sample were calculated by QIIME 2. Bacterial database used was RDP version 11.5 rRNA (http://rdp.cme.msu.edu/) accessed on 2 February 2020. Fungal databases used were UNITE version 8 (https://unite.ut.ee//) accessed on 2 February 2020 and PR2 version 1 (https://github.com/vaulot/pr2_database) accessed on 2 February 2020. A Venn diagram was obtained by the Venny tool. The relationship between soil environmental factors and microbial communities was analyzed by performing Spearman’s rank correlation analysis and redundancy analysis (RDA). Bonferroni correction was used for further p-value study. Significant difference analysis was performed by Duncan’s test (p < 0.05) using SPSS (IBM, Chicago, IL, USA, version 22.0) and the relevant figures were made using Microsoft Excel 2010.

3. Results

3.1. Soil Chemical Properties, Yield, and Quality of the First Experiment

The P, K, Ca, and Zn contents of soil with 20% nitrogen reduction in four kinds of bio-organic fertilizers were different (Table S3). The P, K, and Ca contents of N2 and S1 were the highest. The Pn of J2 was significantly higher than other treatments. (Table S4).
Nitrogen reduction of 20% in four different bio-organic fertilizers promoted the growth of non-heading Chinese cabbages. N1, N2, S1, S2, J1, and J2 had an advantageous effect on growth (Tables S5 and S6). Compared with T1, the yields of N2, S2, and J2 were increased by 20.9%, 6.5%, and 19.8%, respectively (Figure 1).

3.2. Soil Chemical Properties, Soil Element Content, and Soil Enzyme Activities of the Second Experiment

The soil pHs of N2 and S2 were significantly higher than that of the conventional fertilization treatment (T1). On the contrary, the EC was lower than in T1. The available phosphorus and ammoniacal nitrogen of N2 were higher than that of T1. The nitrate nitrogen content of N2 and J2 was decreased compared with T1 (Table 2). The FAD enzyme activity of N2 was significantly higher than other treatments (Figure S1). Invertase activity of N2 and S2 showed no significant differences with T1.
The P, K, Ca, and Zn contents of soil have no significant differences among different treatments. However, the K and Zn contents in the N2 plant, and the Ca contents in the J2 plant were significantly higher than in T1 (Tables S7 and S8).

3.3. Soil Microbiomes

The rarefaction curves were close to plateau (Figure S2), indicating that the sequencing depth met the requirements, and the results can truly reflect the sample condition. After quality filtering, 895,811 sequences were clustered into 3663 OTUs with the bacteria, and 1,069,019 sequences were clustered into 1393 OTUs with the fungi.
Chao, Shannon, and Simpson indexes were computed based on the OTUs. For the Simpson index, the larger the value, the lower the community diversity; however, the Shannon index was just the opposite. In this experiment, the Shannon values of N2 of the bacteria decreased compared with conventional fertilization treatment. On the contrary, the Simpson value of fungi increased significantly, indicating that whole chemical fertilizers decreased species’ richness and diversity (Table S9). The Venn diagram revealed the overlapped and unique OTUs with all of the samples. The OTUs shared by all of the samples were 1593, 325, and 132 for the bacteria and fungi (Figure 2a and Figure 3a). There were also 144 and 99 unique OTUs in N2 and 102 and 111 in T1 for the bacteria and fungi, respectively, indicating that fertilizers changed the communities in the soil of non-heading Chinese cabbage. N2 had a lager influence on the bacterial communities than the application of nitrogen fertilizer solely. On the contrary, nitrogen fertilizer had a larger influence on the fungal communities. Bacterial and fungal diversity of the N2 soil was increased compared with T1.
At the phylum level (Figure 2b), the dominant bacterial phyla in all of the samples were Proteobacteria, Actinobacteria, Chloroflex, Acidobacteria, Bacteroidetes, Firmicute, Planctomycetes, Cyanobacteria, and Gemmatimonadetes. Proteobacteria was the most abundant phylum, followed by Acidobacteria and Chloroflex. The Proteobacteria (32.23%) and Bacteroidetes (7.66%) contents of S2 in soil were both increased compared with CK. The Firmicutes of CK (5.33%) was decreased compared with other treatments. In addition, the Gemmatimonadetes content of N2 increased by 47.86% compared with T1. The dominant fungal phyla of all samples were Ascomycota, Mortierellomycota, Basidiomycota, and Olpidiomycota. Among them, Ascomycota was the most abundant. With fertilizers, Ascomycota decreased compared with the non-fertilization treatment. In addition, the Ascomycota content of N2 decreased by 45.47% compared with T1 (Figure 3b).
The RDA results of the bacterial and fungal communities were showed in Figure 2 and Figure 3 (Figure 2c and Figure 3c). They suggested that the first two RDA components explain 52.04 and 14.45% of the total variance in the bacterial community (RDA1 and RDA2) (Figure 2c), and 44.59 and 27.90% in the fungal community (RDA1 and RDA2) (Figure 3c). Furthermore, we calculated the p-values to investigate the significance effects of soil environmental factors on microbial community composition. Among the factors, AP (p = 0.007) and UREA (p = 0.02) had significant influence on the fungal community structure. OM (p = 0.022) indicated that microbial community compositions of soil were strongly affected by AP, UREA, and OM after fertilizers were applied.
At the genus level (Figure 2d), the top nine of the dominant bacterial genera of all samples were Arthrobacter, Massilia, Nocardioides, Ramlibacter, Dyella, norank_o_Acidobacteriales, Gemmatimonas, Bacillus, and Rhodanobacter. Additionally, Arthrobacter, Gemmatimonas, and Bacillus of N2 were increased compared with CK. Burkholderia-Caballeronia-Parabulkholderia of T2 was increased compared with CK. The top nine dominant fungal genera of all samples were Fusarium, Mortierella, Saitozyma, Humicola, Guehomyces, Penicillium, Plectosphaerella, Solicoccozyma, and Aspergillus. In addition, Fusarium, Saitozyma, and Humicola of N2 were decreased compared with other treatments. On the contrary, Mortierella and Pseudouralinia increased (Figure 3d).
Moreover, the Spearman’s correlation analysis results revealed the relationships between the genus level and the environmental factors (Figure 2e and Figure 3e). In the bacterial community, ACP had extremely significant negative correlation with Streptomyces (punadj = 0.00414), FDA had extremely significant negative correlation with Burkholderia-Caballeronia-Paraburkholderia (punadj = 0.00207), NO3–N had extremely significant positive correlation with Burkholderia-Caballeronia-Paraburkholderia (punadj = 0.00108), and UREA had significant positive correlation with Rhodanobacter (punadj = 0.00691). In the fungal community, INV had extremely significant negative correlation with Aspergillus (punadj = 0.00277) and Epicoccum (punadj = 0.00871). FDA and pH had significant positive correlation with Olpidium (punadj = 0.00625, punadj = 0.00372). The results of Spearman’s correlation analysis revealed the relationships between genus level and the yield and nitrate content (Figure 2f and Figure 3f). In the bacterial community, yield had significant positive correlation with Rhodanobacter (punadj = 0.02606). In the fungal community, yield had significant positive correlation with Olpidium (punadj = 0.00536).

3.4. Vitality of the Root, Photosynthetic Characteristics, Quality, Growth, and Yield of the Second Experiment

The root vitality of N2 and S2 were higher than T1 (Figure S3). Pn, Gs, and Tr of N2 were significantly higher than T1 (Table S10). The soluble sugar content and cellulose of CK were higher than other treatments (Table 3). The VC content of N2 was increased; however, on the contrary, the nitrate content was decreased and significantly lower than T1. The soluble protein and nitrate content of J2 was the highest and significantly higher than T1. Nitrogen reduction with bio-organic fertilizer significantly increased cabbage growth compared with chemical fertilizer treatment solely. The plant height and petiole length of N2 and S2 were significantly higher than T1 (Table S11). The yield of N2 and S2 increased by 9.24% and 6.93%, respectively, compared with T1 (Figure S4). The data of the yield showed the same trend with the third and fourth experiment we conducted (Qi. et al. 2021). Correlation analysis illustrated that the yield was positively correlated with root vitality (p < 0.05), total chlorophyll (p < 0.01), soil pH (p < 0.05), and soil OM (p < 0.05), and was negatively correlated with soluble sugar (p < 0.01) (Table 4).

4. Discussion

Our results showed not only the soil properties and soil community composition, but also the quality and the yield of non-heading Chinese cabbage that were significantly influenced by nitrogen reduction with different bio-organic fertilizers, especially with the No.1 bio-organic fertilizer (Figure 2 and Figure 3, Table 3).

4.1. Effects of Nitrogen Reduction with Bio-Organic Fertilizer on Soil Chemical Properties

Many studies indicated that a favorable environment was the prerequisite for high yield and outstanding quality of crops, and different nitrogen sources had enormous effects on soil character [33,34,35]. In this experiment, 20% nitrogen reduction with bio-organic fertilizers increased the pH, organic matter, available phosphorus, and total nitrogen content. Appropriate soil pH is beneficial for agricultural production, and organic farming could increase soil pH when compared to conventional farming in acidic soils [36], whereas the application of mineral fertilizer decreased soil acidity by acidification and nitrification [37]. In our study, a reduced mineral fertilizer combined with bio-organic fertilizers increased soil pH in acidic soil (Table 2). In the second experiment, in the case of the same total nitrogen application, the total soil nitrogen content, available phosphorus, and soil organic matter content of N2 (bio-organic fertilizer with Bacillus) were significantly higher than in other treatments (Table 2). We found that the organic matter and available phosphorus content of N2 soil increased by 11.95% and 106.45%, respectively, compared with T1 (all chemical fertilization). Ye et al. [3] also found that Trichoderma-enriched bio-organic fertilizer significantly enriched soil fertility, as the soil organic matter, total N, total P, and total K all increased. Research suggests that organic matter as an overall indicator is essential for soil quality, which can bring many benefits to soil and plants [38]. The application of organic fertilizer not only improves soil enzyme activity [39], but also improves the available macronutrient content and increases soil micronutrient availability [40]. In this study, nitrogen reduction with bio-organic fertilizer improved the invertase and FDA soil activities (N2 and S2) (Figure S1), as well as K and Zn contents (N2) compared with conventional fertilization. In chili and cotton, application of Bacillus also increased soil invertase and FDA activities [41,42].

4.2. Effects of Nitrogen Reduction with Bio-Organic Fertilizer on the Soil Microbial Community

Fertilization had an essential impact on the composition of the soil microbe community of cabbage (Figure 2). In general, bio-organic fertilizer increased the proportion of beneficial microorganisms and decreased the proportion of harmful microorganisms, which in turn improved soil biofertility. Previous research showed that fertilizers could change the dominant bacterial and fungal phyla of soil [43,44]. In this experiment, the relative proportions of Proteobacteria and Bacteroidetes were all increased, and especially the relative proportion of Gemmatimonadetes of N2 increased compared with T1. Proteobacteria is known as halophilic bacteria with hydrolase activities [45,46]. Some chemical fertilizer-associated rhizobacteria were related to the degradation of organic substances such as Bacteroidetes [3]. Gemmatimonadetes and Bacteroidetes are essential for soil carbon cycling, which could improve the soil C/N [47,48]. Ascomycota decreased significantly after applying fertilizers, which was consistent with the results of the studies by Feng et al. [49]. Dyella spp. was involved in the Se biogeochemical cycle [50]. Bradyrhizobium was a kind of nitrogen-fixing bacteria related to nitrogen fixation [51]. Mortierella dissolved insoluble phosphorus by releasing a variety of organic acids in soil and promoted phosphorus cycling [52]. Mortierella promoted plant growth by improving soil phosphatase activity [53]. Humicola had a strong decomposition effect on organic matter [54]. Fusarium caused a variety of plant diseases, such as root rot, and decreased the yield and quality of crops [55].
Microbial community composition of the soil was correlated with AP, UREA, OM, and INV after applying bio-organic fertilizers (Figure 2e and Figure 3e). Abundances of several microbial phyla (e.g., Proteobacteria, Bacteroidetes, and Gemmatimonadetes) were mainly influenced by the soil’s available nutrients [56,57]. The application of fertilizer increases soil organic matter and alters microbial community structure and keystone taxa [58]. In the experiment, ACP had extremely significant negative correlation with Streptomyces, and FDA had extremely significant negative correlation with Burkholderia-Caballeronia-Paraburkholderia and Olpidium. Organic amendment and mineral fertilizer affected the soil invertase activity and microbial functional diversity [59]. At the genus level, soil pH is maybe the most important factor that has notable influences on the structure of soil bacterial communities [10]. In this experiment, pH had significant positive correlation with Olpidium.

4.3. Effects of Nitrogen Reduction with Bio-Organic Fertilizer on the Growth, Yield, and Quality of Non-Heading Chinese Cabbage

The experiment indicated that nitrogen reduction with “No.1” was beneficial to improve the growth, yield, and quality of the cabbage. Efficiency of crop photosynthesis was improved by suitable nutrient supply [60]. We found that the Pn of J2 and S2 was increased compared with T1 in the first experiment (Table S4), and Pn, Gs, and Tr of N2 were increased in the second experiment (Table S10). The results also illustrated that total chlorophyll content was positively correlated with the yield (Table 4). The P, K, and Ca contents of N2 were the highest and significantly higher than in CK. The accumulation and formation of plant dry matter was closely related to nitrogen, and nitrogen was closely related to the growth, development, and yield of vegetables [61]. Research also illustrated that organic fertilizer with Bacillus content could reshape the soil community structure and benefit the growth of cabbage [44]. Bacillus is a kind of probiotic, which can secrete plant hormones and promote plant growth [62]. In addition, nitrogen reduction with bio-organic fertilizer (N2, S2) can improve root vitality (Figure S4). We found that root vitality was positively correlated with yield (Table 4). Such well-developed roots could give a foundation for the development of aboveground parts and accumulation of biomass by providing favorable conditions and improve nutrient and water absorption for non-heading Chinese cabbage [63]. The application of bio-organic fertilizer may also stimulate enzyme secretion by the roots [9]. Therefore, in this study, compared with T1 (100% chemical fertilizer), the yield of N2 (total N reduced 20% with No.1) increased by 10.20%, 20.90%, and 9.24% in the two experiments by different non-heading Chinese cabbage cultivars (Figure 1 and Figure S4). In general, the yield was positively correlated with soil pH, organic matter, root vitality, and total chlorophyll (Table 4). Moreover, the yield had significant positive correlation with Rhodanobacter and Olpidium. Rhodanobacter is an essential clade involved in denitrification of acidic soils [64].
The soluble sugar and VC content in non-heading Chinese cabbage of S2 and J2 were also significantly higher than in T1 in the first experiment (Figure S1). On the contrary, the nitrate content of N2 was decreased and significantly lower than T1. Similar results were reported by Wang [65] and Qi [66]. Feng et al. [67] also found that Bacillus megaterium enriched bio-organic fertilizer, significantly increased the vitamin C content, and decreased the nitrite content in Chinese flowering cabbage. Nitrogen was the key factor which could influence the nitrate content in vegetables. In addition, nitrate was a precursor for the synthesis of nitrosamines, which damages people’s health with excessive intake [68]. A total of 85–90% of an adult’s dietary intake of NO3− is from vegetables, as the vegetables tend to have a concentration of NO3− due to the accumulation of nitrogen fertilizer in the soil [69,70]. Therefore, replacing nitrogen with bio-organic fertilizer can reduce the accumulation of nitrogen in vegetables and, in turn, can lower the risks of some nitrate-related health problems.

5. Conclusions

The results illustrated that the application of Bacillus enriched bio-organic fertilizer No.1 succeeded in avoiding the overuse of mineral fertilizers to a significant extent without compromising the yield. More importantly, 20% reduced nitrogen with No.1 led to the improvement of soil pH, organic matter, soil microbial environment, and associated factors, as well as plant photosynthesis and root activity. This in turn promoted the yield and VC contents and declined the nitrate content of non-heading Chinese cabbage. For the soil microbial environment, the dominant phyla of Gemmatimonadetes and Chytridiomycota increased significantly, whereas Ascomycota decreased. The dominant genera Gemmatimonas and Bacillus increased, whereas Fusarium decreased. Redundancy analysis showed that the AP, OM, UREA, and INV of the soil were significantly correlated with the microbial community structure.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12061437/s1, Figure S1: Soil-enzyme activities at the root soil of cabbage under different fertilization treatments; Figure S2: Dilution curve of (a,d) bacteria, (b,e) fungi species abundance Alpha diversity index of soil samples; Figure S3: Effects of bio-organic fertilizer with nitrogen reduction on root vitality; Figure S4: Effects of bio-organic fertilizer with nitrogen reduction on yield of non-heading Chinese cabbage; Figure S5: Field growth status of non-nodular Chinese cabbage; Table S1: Fertilization situation in first experiment; Table S2: Information of primers used in this study; Table S3: Effect of nitrogen reduction by 20% combined with bio-organic fertilizer on five elements in soil of cabbage; Table S4: Effects of different fertilization with nitrogen reduced 20% treatments on photosynthetic characteristics of cabbage; Table S5: Effects of different fertilization with nitrogen reduced 20% treatments on growth of cabbage; Table S6: Effects of different fertilization with nitrogen reduced 30% treatments on growth of cabbage; Table S7: Effects of bio-organic fertilizer with nitrogen reduction on soil element content of non-heading Chinese cabbage; Table S8: Effects of bio-organic fertilizer with nitrogen reduction on element content of the plant; Table S9: Effect of different fertilizer treatments on bacterial, fungi, protist Alpha diversity indexes of soil; Table S10: Effects of bio-organic fertilizer with nitrogen reduction on photosynthetic characteristics of the cabbage; Table S11: Effects of bio-organic fertilizer with nitrogen reduction on growth of the cabbage.

Author Contributions

Y.Q. and F.J. designed the experiments. Y.Q. and Y.C. performed the experiments. Y.Q., L.Y. and R.Z. analyzed the data. Y.Q. wrote the manuscript. X.H. and Z.W. gave valuable comments on the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

We acknowledge The National Key Research and Development Program of China (2018YFD0201200, 2019YFD100190200), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and the Expert Workstation of the China Ministry of Science and Technology.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Gai, X.; Liu, H.; Zhai, L.; Tan, G.; Liu, J.; Ren, T.; Wang, H. Vegetable yields and soil biochemical properties as influenced by fertilization in southern China. Appl. Soil Ecol. 2016, 107, 170–181. [Google Scholar] [CrossRef]
  2. Xin, L.; Li, X.; Tan, M. Temporal and regional variations of China’s fertilizer consumption by crops during 1998–2008. J. Geogr. Sci. 2016, 22, 643–652. [Google Scholar] [CrossRef]
  3. Ye, L.; Zhao, X.; Bao, E.; Li, J.; Zou, Z.; Cao, K. Bio-organic fertilizer with reduced rates of chemical fertilization improves soil fertility and enhances tomato yield and quality. Sci. Rep. 2020, 10, 177. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Zhao, Z.; He, J.; Quan, Z.; Wu, C.; Geisen, S. Fertilization changes soil microbiome functioning, especially phagotrophic protists. Soil Biol. Biochem. 2020, 148, 107863. [Google Scholar] [CrossRef]
  5. Kang, A.; Zhang, N.; Xun, W.; Dong, X.; Xiao, M.; Liu, Z.; Xu, Z.; Feng, H.; Zou, J.; Shen, Q. Nitrogen fertilization modulates beneficial rhizosphere interactions through signaling effect of nitric oxide. Plant Physiol. 2021, 188, 1129–1140. [Google Scholar] [CrossRef] [PubMed]
  6. Huang, S.; Tang, J.; Li, C.; Zhang, H.; Yuan, S. Reducing potential of chemical fertilizers and scientific fertilization countermeasure in vegetable production in China. J. Plant Nutr. 2017, 23, 1480–1493. [Google Scholar] [CrossRef]
  7. Li, R.; Tao, R.; Ling, N.; Chu, G. Chemical, organic and bio-fertilizer management practices effect on soil physicochemical property and antagonistic bacteria abundance of a cotton field: Implications for soil biological quality. Soil Tillage Res. 2017, 167, 30–38. [Google Scholar] [CrossRef]
  8. Xue, F.; Yan, T.; Yang, L.; Qiao, J. Influences of organic fertilizer application on soil biological properties. Chin. J. Eco-Agric. 2010, 18, 1372–1377. [Google Scholar] [CrossRef]
  9. Bandyopadhyay, K.K.; Misra, A.K.; Ghosh, P.K.; Hati, K.M. Effect of integrated use of farmyard manure and chemical fertilizers on soil physical properties and productivity of soybean. Soil Tillage Res. 2010, 110, 115–125. [Google Scholar] [CrossRef]
  10. Fierer, N. Embracing the unknown: Disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 2017, 15, 579–589. [Google Scholar] [CrossRef]
  11. Cao, Y.; Zhang, Z.; Ling, N.; Yuan, Y.; Zheng, X.; Shen, B.; Shen, Q. Bacillus subtilis SQR9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol. Fertil. Soils 2011, 47, 495–506. [Google Scholar] [CrossRef]
  12. Sun, X.; Xu, Z.; Xie, J.; Hesselberg, T.; Tan, T.; Zheng, D.; Strube, L.; Dragoš, A.; Shen, Q.; Zhang, R.; et al. Bacillus velezensis stimulates resident rhizosphere pseudomonas stutzeri for plant health through metabolic interactions. ISME J. 2011, 16, 774–787. [Google Scholar] [CrossRef] [PubMed]
  13. Chen, L.; Yang, X.; Raza, W.; Li, J.; Liu, Y.; Qiu, M.; Zhang, F.; Shen, Q. Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Appl. Microbiol. Biotechnol. 2011, 89, 1653–1663. [Google Scholar] [CrossRef] [PubMed]
  14. Cai, F.; Pang, G.; Li, R.; Li, R.; Gu, X.; Shen, Q.; Chen, W. Bioorganic fertilizer maintains a more stable soil microbiome than chemical fertilizer for monocropping. Biol. Fertil. Soils 2017, 53, 861–872. [Google Scholar] [CrossRef]
  15. Gao, M.; Yang, J.; Liu, C.; Gu, B.; Han, M.; Li, J.; Li, N.; Liu, N.; An, N.; Dai, J.; et al. Effects of long-term biochar and biochar-based fertilizer application on brown earth soil bacterial communities. Agric. Ecosyst. Environ. 2020, 309, 107285. [Google Scholar] [CrossRef]
  16. Li, J.; Li, S.; Li, Q. Effects of different amounts of fulvic acid on tomato yield and quality. J. Agric. 2022, 12, 54–59. [Google Scholar]
  17. Hou, X.; Song, X. Research and utilization of Brassica campestris ssp. chinensis Makino (non-heading Chinese cabbage) germplasm resources. J. Nanjing Agric. Univ. 2012, 35, 35–42. [Google Scholar]
  18. Ding, H.; Fan, J.; Jia, C.; Qin, C.; Yang, Y.; Zhang, H.; Zhang, F.; Wen, C.; Yu, S.; Xu, Y. Current situation and trend of vegetable seed industry development in China. China Veg. 2020, 9, 1–8. [Google Scholar]
  19. Raigón, M.D.; García, M.; Maquieira, A.; Puchades, R. Determination of available nitrogen (nitic and ammoniacal) in soils by flow-injection analysis. Analysis 1992, 20, 483–487. [Google Scholar] [CrossRef]
  20. Wang, Q.; Ren, Y.; Meng, L.; Hong, L.; Hui-Min, F.; Wang, H. Simultaneous determination of total nitrogen and organic carbon in soil with an elemental analyzer. Chin. J. Anal. Lab. 2013, 32, 41–45. [Google Scholar]
  21. Bao, S.D. Analysis Method of Soil and Agricultural Chemistry; China Agricultural Press: Beijing, China, 2000; pp. 25–108. [Google Scholar]
  22. Falciani, R.; Novaro, E.; Marchesini, M.; Gucciardi, M. Multi-element analysis of soil and sediment by icp-ms after a microwave assisted digestion method. J. Anal. At. Spectrom. 2000, 15, 561–565. [Google Scholar] [CrossRef]
  23. Sun, X.; Zhu, L.; Wang, J.; Wang, J.; Su, B.; Liu, T.; Zhang, C.; Gao, C.; Shao, Y. Toxic effects of ionic liquid 1-octyl-3-methylimidazolium tetrafluoroborate on soil enzyme activity and soil microbial community diversity. Ecotoxicol. Environ. Saf. 2017, 135, 201208. [Google Scholar] [CrossRef]
  24. Guan, S.Y. Methodology of soil enzyme measurement. In Methods of Soil Enzymology; Guan, Y., Ed.; China Agricultural Press: Beijing, China, 1986; pp. 274–314. [Google Scholar]
  25. Taylor, J.P.; Wilson, B.; Mills, M.S.; Burns, R.G. Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques. Soil Biol. Biochem. 2002, 34, 387–401. [Google Scholar] [CrossRef]
  26. Bates, S.; Berg-Lyons, D.; Caporaso, J.; Walters, W.; Knight, R.; Fierer, N. Examining the global distribution of dominant archaeal populations in soil. ISME J. 2011, 5, 908–917. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Rousk, J.; Baath, E.; Brookes, P.; Lauber, C.; Lozupone, C.; Caporaso, J.; Knight, R.; Fierer, N. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 2010, 4, 1340–1351. [Google Scholar] [CrossRef] [PubMed]
  28. Arono, D.I. Copper enzymes in isolated chloroplasts, polyphenol oxidase in Brta vulgaris. Plant Physiol. 1949, 24, 1–15. [Google Scholar] [CrossRef] [Green Version]
  29. Clemensson, A.; Persson, H. Fine-root vitality in a nor way spruce stand subjected to various nutrient supplies. Plant Soil 1995, 168, 167–172. [Google Scholar] [CrossRef]
  30. Cataldo, D.A.; Maroon, M.; Schrader, L.E.; Youngs, A.L. Rapid colorimetric determination of nitrate in plant-tissue by nitration of salicylic-acid. Commun. Soil Sci. Plant Anal. 1975, 6, 7–80. [Google Scholar] [CrossRef]
  31. Zhang, J.; Kirkham, M.B. Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol. 1996, 132, 361–373. [Google Scholar] [CrossRef]
  32. Buysse, J.A.N.; Merckx, R. An improved colorimetric method to quantify sugar content of plant tissue. J. Exp. Bot. 1993, 44, 1627–1629. [Google Scholar] [CrossRef]
  33. Eltun, R.; Korsth, A.; Nordheim, O. A comparison of environmental, soil fertility, yield, and economical effects in six cropping systems based on an 8-year experiment in Norway. Agric. Ecosyst. Environ. 2002, 90, 155–168. [Google Scholar] [CrossRef]
  34. Bozkurt, S.; Agca, N.; Odemis, B. Influence of different nitrogen sources and leaching practices on soil chemical properties under tomato vegetation in a greenhouse. J. Agron. 2008, 7, 210–219. [Google Scholar] [CrossRef] [Green Version]
  35. Youssef, I.; Ali, M.; Noufal, E.; Ismail, S.; Ali, M. Effect of different sources and levels of nitrogen fertilizers with and without organic and bio-fertilizers on growth and yield components of fennel plants (foeniculum vulgare mill.). Asian J. Soil Sci. Plant Nutr. 2020, 6, 6–14. [Google Scholar] [CrossRef]
  36. Whalen, J.; Chang, C.; Clayton, G.; Carefoot, J. Cattle manure amendments can increase the pH of acid soils. Soil Sci. Soc. Am. J. 2000, 64, 962–966. [Google Scholar] [CrossRef] [Green Version]
  37. Gu, Y.; Wang, Y.; Lu, S.; Xiang, Q.; Yu, X.; Zhao, K.; Zou, L.; Chen, Q.; Tu, S.; Zhang, X. Long-term fertilization structures bacterial and archaeal communities along soil depth gradient in a paddy soil. Front. Microbiol. 2017, 8, 1516. [Google Scholar] [CrossRef] [Green Version]
  38. López, A.; Fenoll, J.; Hellín, P.; Flores, P. Physical characteristics and mineral composition of two pepper cultivars under organic, conventional and soilless cultivation. Sci. Hortic. 2013, 150, 259–266. [Google Scholar] [CrossRef]
  39. Yang, P.; Jian, L.; Sohail, H.; Yu, J.; Li, J. Partial substitution of mineral fertilizer with biofertilizer enhances cauliflower nutritional quality, yield, and soil characteristics. Crop Sci. 2020, 60, 934–944. [Google Scholar] [CrossRef]
  40. Li, B.; Zhou, D.; Cang, L.; Zhang, H.; Fan, X.; Qin, W. Soil micronutrient availability to crops as affected by long-term inorganic and organic fertilizer applications. Soil Tillage Res. 2007, 96, 66–173. [Google Scholar] [CrossRef]
  41. Gou, J.Y.; Suo, S.Z.; Shao, K.Z.; Zhao, Q.; Rensing, C. Biofertilizers with beneficial rhizobacteria improved plant growth and yield in chili (Capsicum annuum L.). World J. Microbiol. 2020, 36, 86. [Google Scholar] [CrossRef]
  42. Wang, N.; Nan, H.; Feng, K. Effects of reduced chemical fertilizer with organic fertilizer application on soil microbial biomass, enzyme activity and cotton yield. J. Appl. Ecol. 2020, 31, 173–181. [Google Scholar]
  43. Liao, J.; Ye, J.; Liang, Y.; Khalid, M.; Huang, D. Pakchoi antioxidant improvement and differential rhizobacterial community composition under organic fertilization. Sustainability 2019, 11, 2424. [Google Scholar] [CrossRef] [Green Version]
  44. Gao, Z.; Han, M.; Hu, Y.; Li, Z.; Ma, Z. Effects of continuous cropping of sweet potato on the fungal community structure in rhizospheric soil. Front. Microbiol. 2019, 10, 2269. [Google Scholar] [CrossRef] [PubMed]
  45. Tang, J.; Zheng, A.; Bromfield, E.; Zhu, J.; Li, S.; Wang, S.; Deng, Q.; Li, P. 16S rRNA gene sequence analysis of halophilic and halotolerant bacteria isolated from a hypersaline pond in Sichuan, China. Ann. Microbiol. 2011, 61, 375–381. [Google Scholar] [CrossRef]
  46. Kami, K.; Ghane, M.; Bababeekhou, L. Hydrolase-producing moderately halophilic bacteria from eshtehard desert (iran). Microbiology 2020, 89, 769–777. [Google Scholar] [CrossRef]
  47. Zhang, H. Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int. J. Syst. Evol. Microbiol. 2003, 53, 1155–1163. [Google Scholar] [CrossRef]
  48. Nemergut, D.R.; Townsend, A.R.; Sattin, S.R.; Freeman, K.R.; Fierer, N.; Neff, J.C.; Bowman, W.D.; Schadt, C.W.; Weintraub, M.N.; Schmidt, S.K. The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: Implications forcarbon and nitrogen cycling. Environ. Microbiol. 2010, 10, 3093–3105. [Google Scholar] [CrossRef]
  49. Feng, C.; Yue, S.; Jian, A.; Chen, L.; Guo, Y.; Zheng, R.; Su, J. The effect of continuous cropping of selenium melon on soil fungal community structure. Chin. J. Eco-Agric. 2019, 10, 2269. [Google Scholar]
  50. Luo, X.; Wang, Y.; Li, Y.; An, j.; Wang, G.; Li, M.; Zheng, S. Microbial oxidation of organic and elemental selenium to selenite. Sci. Total Environ. 2022, 833, 155203. [Google Scholar] [CrossRef]
  51. Lajudie, P. Polyphasic Taxonomy of Rhizobia: Emendation of the genus sinorhizobium and description of Sinorhizobium meliloti comb. nov. Sinorhizobium saheli sp. nov. and Sinorhizobium teranga sp. nov. Int. J. Syst. Bacteriol 1994, 44, 715–733. [Google Scholar] [CrossRef]
  52. Osorio, N.W.; Habte, M. Soil phosphate desorption induced by a phosphate-solubilizing fungus. Commun. Soil Sci. Plant Anal. 2014, 45, 451–460. [Google Scholar] [CrossRef]
  53. Zhang, H.; Wu, X.; Gang, L.; Qin, P. Interactions between arbuscular mycorrhizal fungi and phosphate-solubilizing fungus (Mortierella sp.) and their effects on Kostelelzkya virginica growth and enzyme activities of rhizosphere and bulk soils at different salinities. Biol. Fertil. Soils 2011, 47, 543–554. [Google Scholar] [CrossRef] [Green Version]
  54. Malik, K.; Sandhu, G. Decomposition of organic matter by fungi in saline soils. Mycopathol. Mycol. Appl. 1973, 50, 339–347. [Google Scholar] [CrossRef] [PubMed]
  55. Hu, G. Discussion on the origin of sweet potato root rot in China. J. Henan Univ. Sci. Technol. (Agric. Ed.) 1984, 1, 10–13. [Google Scholar]
  56. Shen, Z.; Wang, D.; Ruan, Y.; Xue, C.; Zhang, J.; Li, R.; Shen, Q. Deep 16S rRNA pyrosequencing reveals a bacterial community associated with banana Fusarium wilt disease suppression induced by bioorganic fertilizer application. PLoS ONE 2014, 9, e98420. [Google Scholar] [CrossRef]
  57. Zhao, J.; Zhang, R.; Xue, C.; Xun, W.; Sun, L.; Xu, Y.; Shen, Q. Pyrosequencing reveals contrasting soil bacterial diversity and com-munity structure of two main winter wheat cropping systems in China. Microb. Ecol. 2014, 67, 443–453. [Google Scholar] [CrossRef]
  58. Lin, Y.; Ye, G.; Kuzyakov, Y.; Liu, D.; Fan, J.; Ding, W. Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol. Biochem. 2019, 134, 187–196. [Google Scholar] [CrossRef]
  59. Hu, J.; Lin, X.; Wang, J.; Dai, J.; Chen, R.; Zhang, J.; Ming, H. Microbial functional diversity, metabolic quotient, and invertase activity of a sandy loam soil as affected by long-term application of organic amendment and mineral fertilizer. J. Soils Sediments 2011, 11, 271–280. [Google Scholar] [CrossRef]
  60. Mauromicale, G.; Ierna, A.; Marchese, M. Chlorophyll fluorescence and chlorophyll content in field-grown potato as affected by nitrogen supply, genotype, and plant age. Photosynthetica 2006, 44, 76. [Google Scholar] [CrossRef]
  61. Fan, M.; Shen, J.; Yuan, L.; Jiang, R.; Zhang, F. Improving crop productivity and resource use efficiency to ensure food security and environmental quality in China. J. Exp. Bot. 2012, 63, 13–24. [Google Scholar] [CrossRef]
  62. Acon, C.; Palencia, E.; Hinton, D. Abiotic and biotic plant stress-tolerant and beneficial secondary metabolites produced by endophytic Bacillus species. In Plant Microbes Symbiosis: Applied Facets; Springer: New Delhi, India, 2015; pp. 163–177. [Google Scholar] [CrossRef]
  63. Gomes, F.; Moraes, J.; Santos, C.; Goussain, M. Resistance induction in wheat plants by silicon and aphids. Sci. Agric. 2005, 62, 547–551. [Google Scholar] [CrossRef]
  64. Van, R.; Van, E.; Jetten, M.; Hefting, M.; Kartal, B. De-nitrification at pH 4 by a soil-derived Rhodanobacter-dominated community. Environ. Microbiol. 2010, 12, 3264–3271. [Google Scholar] [CrossRef]
  65. Wang, Y. Effects of Nitrogen Fertilizer Reduction on Yield and Quality of Non-Heading Chinese Cabbage; Nanjing Agricultural University: Nanjing, China, 2017. [Google Scholar]
  66. Qi, Y.; Jiang, F.; Zhou, R.; Wu, Y.; Hou, X.; Li, J.; Lin, W.; Wu, Z. Effects of reduced nitrogen with bio-organic fertilizer on soil properties, yield and quality of non-heading Chinese cabbage. Agronomy 2021, 11, 2196. [Google Scholar] [CrossRef]
  67. Feng, N.; Liang, Q.; Feng, Y.; Xiang, L.; Wong, M. Improving yield and quality of vegetable grown in paes-contaminated soils by using novel bioorganic fertilizer. Sci. Total Environ. 2020, 739, 139883. [Google Scholar] [CrossRef] [PubMed]
  68. Briseis, A.; Xiao, O.; Yu, T.; Bu, T.; Gong, Y.; Hong, L.; Nathaniel, R.; Wong, H.; Mary, H. Thyroid cancer risk and dietary nitrate and nitrite intake in the Shanghai women’s health study. Int. J. Cancer 2013, 132, 897–904. [Google Scholar] [CrossRef]
  69. Simion, V.; Cmpeanu, G.; Vasile, G.; Artimon, M.; Negoi, M. Nitrate and nitrite accumulation in tomatoes and derived products. Rom. Biotechnol. Lett. 2008, 13, 3785–3790. [Google Scholar] [CrossRef]
  70. Siciliano, J.; Krulick, S.; Heisler, E.G.; Schwartz, J.H.; White, J.W. Nitrate and nitrite content of some fresh and processed market vegetables. J. Agric. Food Chem. 1975, 23, 461–464. [Google Scholar] [CrossRef]
Agronomy 12 01437 g001 550
Figure 1. Effects of different fertilization treatments on the yield of cabbage. Note: (a) 20% reduction of total nitrogen with different bio-organic fertilizer, (b) 30% reduction of total nitrogen with different bio-organic fertilizer. Different small letters represent a significant difference at 0.05 level by Duncan’s test.
Figure 1. Effects of different fertilization treatments on the yield of cabbage. Note: (a) 20% reduction of total nitrogen with different bio-organic fertilizer, (b) 30% reduction of total nitrogen with different bio-organic fertilizer. Different small letters represent a significant difference at 0.05 level by Duncan’s test.
Agronomy 12 01437 g001
Agronomy 12 01437 g002 550
Figure 2. Number of common and unique OTUs based on bacteria (a) Venn analysis; relative abundances of bacteria (b) at the phylum level; redundancy analysis of the five (blue line) dominant bacteria (c) associated with soil properties; relative abundances of bacteria (d) at the genus level; the heatmap of the correlation between the top 20 dominant bacterial (e) genera associated with soil properties; the heatmap of the correlation between the top 20 dominant bacterial (f) genera associated with yield and nitrate content. Note: * at the 0.05 level (double-tailed), the correlation between them was significant; ** at 0.01 level (double-tailed), the correlation between them was significant. TN: soil total nitrogen content, NO3−: soil nitrate nitrogen content, OM: soil organic matter, ACP: acid phosphatase activity, AP: available phosphorus, TOC: total C, NH4–N: ammonium nitrogen, UREA: urease activity of soil, INV: invertase activity, FDA: fluorescein diacetate activity.
Figure 2. Number of common and unique OTUs based on bacteria (a) Venn analysis; relative abundances of bacteria (b) at the phylum level; redundancy analysis of the five (blue line) dominant bacteria (c) associated with soil properties; relative abundances of bacteria (d) at the genus level; the heatmap of the correlation between the top 20 dominant bacterial (e) genera associated with soil properties; the heatmap of the correlation between the top 20 dominant bacterial (f) genera associated with yield and nitrate content. Note: * at the 0.05 level (double-tailed), the correlation between them was significant; ** at 0.01 level (double-tailed), the correlation between them was significant. TN: soil total nitrogen content, NO3−: soil nitrate nitrogen content, OM: soil organic matter, ACP: acid phosphatase activity, AP: available phosphorus, TOC: total C, NH4–N: ammonium nitrogen, UREA: urease activity of soil, INV: invertase activity, FDA: fluorescein diacetate activity.
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Agronomy 12 01437 g003 550
Figure 3. Number of common and unique OTUs based on fungal (a) Venn analysis; relative abundances of fungi (b) at the phylum level; redundancy analysis of the five (blue line) dominant fungi (c) associated with soil properties; relative abundances of fungi (d) at the genus level; the heatmap of the correlation with the top 20 dominant fungal (e) genera associated with soil properties; the heatmap of the correlation with the top 20 dominant fungal (f) genera associated with yield and nitrate content. Note: * at the 0.05 level (double-tailed), the correlation between them was significant; ** at 0.01 level (double-tailed).
Figure 3. Number of common and unique OTUs based on fungal (a) Venn analysis; relative abundances of fungi (b) at the phylum level; redundancy analysis of the five (blue line) dominant fungi (c) associated with soil properties; relative abundances of fungi (d) at the genus level; the heatmap of the correlation with the top 20 dominant fungal (e) genera associated with soil properties; the heatmap of the correlation with the top 20 dominant fungal (f) genera associated with yield and nitrate content. Note: * at the 0.05 level (double-tailed), the correlation between them was significant; ** at 0.01 level (double-tailed).
Agronomy 12 01437 g003
Table
Table 1. Fertilization situation in second experiment.
Table 1. Fertilization situation in second experiment.
TreatmentMineral FertilizerBio-Organic Fertilizer
N
kg·ha−1		P2O5
kg·ha−1		K2O
kg·ha−1		No.1
kg·ha−1		Seek
kg·ha−1		Jiajiapei
kg·ha−1
No fertilizer (CK)------
Conventional fertilizer (T1)193.2135135---
−N20% (T2)154.5135135---
−N20% + No.1 (N2)109.5601251500--
−N20% + Seek (S2)109.560125-1500-
−N20% + Jiajiapei (J2)140.1120.6127.8--720
Table
Table 2. Effects of nitrogen reduction combined with biological organic fertilizer on soil’s physical and chemical properties of non-heading Chinese cabbage.
Table 2. Effects of nitrogen reduction combined with biological organic fertilizer on soil’s physical and chemical properties of non-heading Chinese cabbage.
TreatmentpHEC
ms·m−1		Organic Matter
g·kg−1		Available Phosphorus g·kg−1Total Nitrogen g·kg−1Ammonium Nitrogen g·kg−1Nitrate Nitrogen g·kg−1Organic Carbon
g·kg−1
CK5.15 ± 0.04 bc75.2 ± 7.15 e13.47 ± 0.37 b18.45 ± 1.14 b1.80 ± 0.02 b5.70 ± 1.63 ab8.78 ± 0.19 d8.06 ± 0.3 b
TI5.14 ± 0.07 c148.60 ± 6.03 a16.44 ± 1.44 ab31.45 ± 5.10 b1.81 ± 0.04 b4.50 ± 0.18 b18.95 ± 0.52 a9.54 ± 0.84 ab
T25.18 ± 0.03 bc111.27 ± 5.46 ab15.57 ± 0.39 ab30.58 ± 2.5 b1.85 ± 0.03 b8.34 ± 1.04 ab15.80 ± 0.47 b9.03 ± 0.23 ab
N25.38 ± 0.04 a92.83 ± 8.94 de18.07 ± 0.31 a64.93 ± 3.07 a2.07 ± 0.02 a12.57 ± 2.69 a11.29 ± 0.57 c10.59 ± 0.13 a
S25.32 ± 0.04 ab95.23 ± 10.65 ed17.08 ± 1 ab22.80 ± 2.87 b1.80 ± 0.01 b5.68 ± 0.95 ab11.18 ± 0.24 c9.91 ± 0.58 a
J25.07 ± 0.03 c134.67 ± 2.34 ab14.88 ± 0.45 ab21.82 ± 1.76 b1.83 ± 0.04 b7.18 ± 0.64 ab9.40 ± 0.72 d9.79 ± 0.55 a
Note: CK is no fertilization, T1 is 100% fertilization, T2 is 20% reduced nitrogen, N2 is 20% reduced nitrogen + 1500 kg·ha−1 “No.1”, S2 is 20% reduced nitrogen +1500 kg·ha−1 “Seek”, J2 is 20% reduced nitrogen + 720 kg·ha−1 “Jiajiapei”. The different small letters represent a significant difference at 0.05 level by Duncan’s test.
Table
Table 3. Effects of bio-organic fertilizer with 20% nitrogen reduction on quality of non-heading Chinese cabbage.
Table 3. Effects of bio-organic fertilizer with 20% nitrogen reduction on quality of non-heading Chinese cabbage.
TreatmentsSoluble Sugar
(mg·g−1)		Cellulose
%		Soluble Protein
(mg·g−1)		Vitamin C
(mg·100 g−1)		Nitrate
(mg·kg−1)
CK1.07 ± 0.03 a27.31 ± 1.36 a10.51 ± 0.34 d68.13 ± 2.45 cd551.83 ± 24.66 bc
T10.53 ± 0.06 bc18.87 ± 0.47 bc11.15 ± 0.38 c69.74 ± 1.38 ab564.04 ± 25.27 b
T20.40 ± 0.05 c16.94 ± 0.40 c11.62 ± 0.12 ab69.61 ± 3.55 ab507.03 ± 42.90 bc
N20.63 ± 0.02 b18.42 ± 1.23 c11.20 ± 0.48 ab73.23 ± 2.36 a446.15 ± 29.04 c
S20.52 ± 0.01 bc19.76 ± 0.42 b10.56 ± 0.27 c72.62 ± 2.77 ab475.03 ± 21.91 bc
J20.56 ± 0.84 bc18.13 ± 1.72 c11.87 ± 0.29 a68.90 ± 2.77 bcd1309.40 ± 52.77 a
Note: CK is no fertilization, T1 is 100% fertilization, T2 is 20% reduced nitrogen, N2 is 20% reduced nitrogen + 1500 kg·ha−1 “No.1”, S2 is 20% reduced nitrogen +1500 kg·ha−1 “Seek”, J2 is 20% reduced nitrogen + 720 kg·ha−1. The different small letters represent a significant difference at 0.05 level by Duncan’s test.
Table
Table 4. Correlation with soil nutrients, yield, and quality of non-heading Chinese cabbage.
Table 4. Correlation with soil nutrients, yield, and quality of non-heading Chinese cabbage.
YieldVCNitrateSoluble
Sugar		Total
Chloro-
phyll		Root
Activity		pHOMTNTPTKTCaTZn
Yield1
VC−0.0981
Nitrate0.0620.3921 1
Soluble
sugar		−0.688 **0.097−0.0781 0.5
Total
chlorophyll		0.804 **−0.3390.09−0.602 **1 0
Root
activity		0.487 *0.196−0.245−0.3870.2891 −0.5
pH0.588 *−0.36−0.624 **−0.2910.4070.4341 −1
OM0.565 *0.2740.071−0.0140.3380.3110.3281
TN0.066−0.0730.1560.0230.0480.201−0.006−0.2931
TP0.007−0.422−0.3360.1710.224−0.0790.363−0.115−0.2231
TK−0.311−0.096−0.408−0.046−0.399−0.045−0.014−0.249−0.3660.0511
TCa−0.203−0.422−0.3460.264−0.026−0.2820.217−0.326−0.3750.856 **0.3231
TZn−0.578 *−0.56 *−0.553 *0.532 *−0.38−0.3010.127−0.273−0.1670.557 *0.4340.692 **1
Note: * at the 0.05 level, the correlation between them was significant; ** at 0.01 level, the correlation between them was significant.
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Qi, Y.; Wu, Z.; Zhou, R.; Hou, X.; Yu, L.; Cao, Y.; Jiang, F. Nitrogen Reduction with Bio-Organic Fertilizer Altered Soil Microorganisms, Improved Yield and Quality of Non-Heading Chinese Cabbage (Brassica campestris ssp. chinensis Makino). Agronomy 2022, 12, 1437. https://doi.org/10.3390/agronomy12061437

AMA Style

Qi Y, Wu Z, Zhou R, Hou X, Yu L, Cao Y, Jiang F. Nitrogen Reduction with Bio-Organic Fertilizer Altered Soil Microorganisms, Improved Yield and Quality of Non-Heading Chinese Cabbage (Brassica campestris ssp. chinensis Makino). Agronomy. 2022; 12(6):1437. https://doi.org/10.3390/agronomy12061437

Chicago/Turabian Style

Qi, Yingbin, Zhen Wu, Rong Zhou, Xilin Hou, Lu Yu, Yuxin Cao, and Fangling Jiang. 2022. "Nitrogen Reduction with Bio-Organic Fertilizer Altered Soil Microorganisms, Improved Yield and Quality of Non-Heading Chinese Cabbage (Brassica campestris ssp. chinensis Makino)" Agronomy 12, no. 6: 1437. https://doi.org/10.3390/agronomy12061437

APA Style

Qi, Y., Wu, Z., Zhou, R., Hou, X., Yu, L., Cao, Y., & Jiang, F. (2022). Nitrogen Reduction with Bio-Organic Fertilizer Altered Soil Microorganisms, Improved Yield and Quality of Non-Heading Chinese Cabbage (Brassica campestris ssp. chinensis Makino). Agronomy, 12(6), 1437. https://doi.org/10.3390/agronomy12061437

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