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Article

Effect of Organic Fertilizer Application on Microbial Community Regulation and Pollutant Accumulation in Typical Red Soil in South China

by
Qinghong Sun
1,2,
Qiao Zhang
1,2,
Zhijie Huang
1,2,
Chang Wei
1,2,
Yongtao Li
1,2 and
Huijuan Xu
1,2,*
1
Key Laboratory of Arable Land Conservation (South China), MOA, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
2
Guangdong Province Key Laboratory for Land Use and Consolidation, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(9), 2150; https://doi.org/10.3390/agronomy14092150
Submission received: 7 August 2024 / Revised: 19 September 2024 / Accepted: 19 September 2024 / Published: 21 September 2024
(This article belongs to the Section Agricultural Biosystem and Biological Engineering)
Browse Figures
Versions Notes

Abstract

:
Returning livestock manure to the cropland as organic fertilizer is a sustainable and environmentally friendly treatment method, but its application also alters the soil microenvironment. However, the impact of soil microbial community disturbance and pollutant accumulation from different types of organic fertilizers remains largely unknown in South China. To fill this gap, we investigated the effects of organic fertilizers, including chicken manure, pig manure and vermicompost on the soil bacterial and fungal communities and environmental risks. The results show that applying organic fertilizer effectively increases the soil nutrient content. High-throughput sequencing of bacteria and fungi showed that the application of different organic fertilizers had differential effects on microbial community structure, with the highest number of microbe-specific OTUs in the vermicomposting treatment. Additionally, this study found no risk of heavy metal (Cu, Zn, Pb, Cr and Cd) contamination from short-term organic fertilizer application, but there was a risk of antibiotic (ENR and CHL) contamination. Functional microorganisms regulating heavy metals and antibiotics were identified by RDA analysis. This study facilitates the screening of types of organic fertilizers that can be safely returned to the field as well as developing strategies to regulate functional microbes.

1. Introduction

Soil microbes are the most abundant and diverse organisms on Earth. They play a crucial role in soil quality through their involvement in nutrient cycling [1], plant nutrition, fitness, and health [2,3]. Soil microorganisms, a key index for evaluating soil quality, are significantly impacted by agricultural management practices such as irrigation and fertilization [4]. Healthy soils provide essential functions and offer social, economic, and ecological benefits, including a livable environment, food security, and ecological balance [5]. Soil microbes regulate soil health processes [6], such as the stabilization of organic matter, the formation of soil aggregates, and the inhibition of plant pathogens [7]. In addition, it is also a factor of soil formation [8]. Studies have shown that soils with higher microbial diversity exhibit more ecological functions, increased resistance to environmental stresses, and enhanced crop productivity [9]. Microbial activity is closely related to soil organic matter, physical properties and enzyme activity, serving as a measure of soil productivity and pollution level [10]. In nitrogen cycling, protists have been found to be more sensitive to nitrogen fertilizer application and seasonal changes than fungi and bacteria, highlighting their importance in the soil microbiome [11]. Importantly, soil functions depend not only on number of species in the community (microbial diversity), but also on the complex interactions among community members [12].
The intensification of agriculture through the excessive use of chemical nitrogen fertilizer has massively increased food production over recent decades [13]. Furthermore, the extensive application of inorganic fertilizers has led to the degradation of ecosystem structure and functions, including soil acidification, reduced nutrient availability, loss of biodiversity, and environmental pollution [14,15]. The partial substitution of synthetic N with organic fertilizers (hereafter referred to as partial organic substitution) is one solution used to improve the sustainability of food systems [16,17]. Recycling nutrients from manure into the soil offers an important alternative to chemical fertilizers and contributes to the greening of agriculture [18]. Partial organic substitution can affect various agroecosystem functions by altering biological composition, activity, and functional gene abundance [19], thereby improving soil fertility increasing crop yield or quality [20]. Research indicates that organic fertilizers can yield results that are either higher or comparable to those achieved with chemical fertilizers. Additionally, repeated applications of cow manure organic fertilizer lead to an increase in soil organic matter. The impact of organic fertilizers on soil pH can vary: while repeated use might cause soil acidification, the organic matter they contain can help buffer against decreases in soil pH [21,22]. Furthermore, organic fertilizers enhance organic carbon storage and sequestration rates, boost soil nutrient retention capacity, improve fertilizer efficiency, and create a more favorable microbial environment for root systems. They also stimulate crop root systems, as well as the secretion of organic acids, amino acids, and sugars, which in turn promotes better nutrient uptake by the crops [23,24,25]. Additionally, the application of organic fertilizers supports enzyme reactions and microbial activity linked to soil nutrient transformations, encourages the proliferation of beneficial microorganisms, and optimizes soil microbiota succession [26,27,28]. Studies have shown that irrigation combined with either chemical or organic fertilization notably increases bacterial populations while significantly reducing the relative abundances of Actinobacteria and Saccharibacteria compared to non-irrigation treatments [29].
Organic fertilizers are rich in nutrients, including organic matter, humus and beneficial microorganisms [30]. The application of organic fertilizers can increase the soil microbial abundance and benefit the functional diversity of soil microorganisms [31,32,33]. Shen et al. [34] observed that the application of organic fertilizers for 20 years caused changes in bacterial community composition of acid soils in Northeast China. And application of organic fertilizers increased the abundance of commensal bacteria such as Proteobacteria or Chloroflexi [31,35]. Likewise, Wu et al. [36] found that fertilizer application altered the abundance and diversity of bacteria in the rhizosphere soil of crops, and the relative abundances of Nitrospira, Pseudomonas, Arthrobacter and Bacillus were significantly elevated by increasing the application of organic fertilizers and reducing the application of chemical fertilizers for two consecutive years. As we all know, the harmful effects of heavy metals on the environment cannot be ignored. The basic characteristics and nutrient structure of the soil polluted by heavy metals are damaged to varying degrees [37]. Prolonged use of livestock manure in agriculture can result in significant accumulation of heavy metals in both soil and plant [38]. To remediate contaminated soils, organic fertilizers, as well as mixtures of organic and inorganic substances, are commonly employed [39,40]. The application of organic fertilizer also has a significant effect on the availability and morphology of heavy metals in soil contaminated by multiple metals [39]. Additionally, research indicates that applying pig manure can reduce the bioavailability of heavy metals [41]. The application of organic fertilizer can not only increase the concentration of Zn in vegetables, but also enhance the level of DPTA-extractable Zn and DGT-extractable Zn in soil [42]. Therefore, the effect of organic fertilizer application process on heavy metals in lateritic red soil needs to be further investigated.
Currently, the effects of the return of livestock and poultry manure organic fertilizer on soil microbial diversity, community disturbance and soil nutrient characteristics in typical red soil in South China remain unknown. Therefore, this study aims to elucidate the mechanism affecting of microbial (bacterial and fungal) communities, diversity and soil nutrient status of lateritic red soil by replacing some chemical nitrogen fertilizers with various livestock and poultry organic fertilizers.

2. Materials and Methods

2.1. Study Site and Experimental Process

This study was carried out at the Yue Tang experimental station (22°65′ N, 112°30′ E), South China Agricultural University, Guangzhou, Guang Dong Province, China. The experiment area has a subtropical monsoon climate with an average annual temperature of 21.6 °C. The annual average sunshine is 1694.8 h, and the annual sunshine percentage is 38%. The average annual rainfall is 1611.0 mm and the average annual evaporation is 1200 mm. The soil type is a typical red soil (WRB Soil classification: plinthosols) in South China. The basic physicochemical properties of the soil were: pH 4.82 ± 0.05, electrical conductivity 8.37 ± 1.31 dS/m, available phosphorus 50.4 ± 2.5 mg/kg, available potassium 56.7 ± 3.1 mg/kg, ammonium nitrogen 15.3 ± 1.1 mg/kg, nitrate nitrogen 3.83 ± 0.17 mg/kg, organic matter 40.7 ± 3.1 g/kg. Different types of livestock and poultry was composted and applied to the test area as organic fertilizer, and water spinach (Ipomoea aquatica Forssk) was used as test crop. Five treatments were set up in the experiment, which were no fertilization (CK), formula fertilizer (FF), earthworm manure + 85% formula fertilizer (EF), chicken manure + 85% formula fertilizer (CF) and pig manure + 85% formula fertilizer (PF). The replacement treatment of organic fertilizer uses the same amount of organic fertilizer to supplement the corresponding reduction in nitrogen fertilizer, that is the replacement of 15% of organic fertilizer is applied according to 7500 kg hm−2 (Table 1). Apply organic fertilizer evenly into the soil before sowing and wait for 7 days before sowing. Each treatment was repeated 3 times, the plot area was 35 m2 (5 m × 7 m), and there were 0.5 m protection lines between the plots, which were arranged by random block design. The basic physicochemical properties of organic fertilizer are shown in Table 2.

2.2. Soil Sampling Collection and Processing

At each plot, 2.5 kg of soil samples was collected from the surface layer (0–20 cm) before sowing and after harvesting [43]. At least 3 subsamples were collected from each plot and then blended into one sample. Finally, each sample is divided into two parts. One part of soil samples was stored in an ultra-low-temperature refrigerator (−80 °C) for the determination of antibiotic content and microbial communities in the soil, and the other part was air-dried and then passed through a mesh sieve with a pore size of 2 mm, 1 mm, and 0.15 mm for the determination of basic soil properties and heavy metal contents, respectively.

2.3. Determination of the Soil Nutrient Index and Pollutant Content

A 1:10 soil/water suspension (w/v) was used to measure soil pH after 1 h of shaking at 25 °C. Soil samples were burned at 550 °C for 2 h for determination of organic matter content (OM). The samples were digested by microwave acid digestion and analyzed by Inductively Coupled Plasma Optical Emission Spectrometer (ICPOES) for available phosphorus (AP) and available potassium (AK) content. Soil samples and 0.01 M CaCl2 solution were used in a 1/10 ratio to obtain suspensions (w/v) for the determination of NH4+-N and NO3−-N [44]. And the heavy metals Pb, Cr, Cd, Cu, Zn in the samples were digested by HNO3-HF-HClO4 method and determined by flame-atomic absorption spectrometry [45]. And soil antibiotics (enrofloxacin: ENR, ciprofloxacin: CIP, tetracycline hydrochloride: TET, chrysin hydrochloride: CHL) were extracted from freeze-dried samples by high performance liquid chromatography [46].

2.4. Soil Micro-Ecological Community Analysis

In this study, the community structure of bacteria and fungi in soil was determined. After the genome was extracted by soil DNA extraction kit, the V3–V4 variable region of 16 SrRNA gene of bacteria and ITS of fungus were amplified and purified with barcode primer, and equal amounts of mixed libraries were constructed. Last, the samples were determination for high-throughput sequencing based on the same scheme produced by the Beijing Novogene Bio-Pharm Technology Co., Ltd. (Beijing, China). The primer sequences used were 338F-806R (5′-ACTCCTACGGGAGGCAGCAG-3′; 5′-GGACTACHVGGGTWTCTAAT-3′) and ITS1F-ITS2R (5′-CTTGGTCATTTA-GAGGAAGTAA-3′; 5′-GCTGCGTTCTTCATCGATGC-3′) [47,48]. The microbial diversity of each soil sample was obtained by alpha diversity analysis. Alpha diversity focuses on the number of species in a homogeneous habitat in a local area, so it is also known as intra-biological diversity. In the analysis, several different alpha diversity indices, observed species, Chao1, Shannon, Simpson and Good coverage, were selected to characterize the diversity and evenness of species distribution in the samples, and visually display the sequencing depth and data volume.

2.5. Statistical Analysis

All original data were processed using Excel 2016. Physicochemical data were analyzed by one-way ANOVA (p < 0.05) and Duncan’s tests using IBM SPSS (Version 22.0, SPSS Inc., Chicago, IL, USA). Origin 2021 and Canoco for windows was used to de-complete histograms, heatmaps, PCA plots and redundancy analysis (RDA). All treatment samples in this study were subjected to triplicate biological replicates determinations.

3. Results

3.1. Effect of Different Organic Fertilizers on Soil Properties and Pollutions Concentration

3.1.1. Changes in OM, AP and AK Content

The soil properties are illustrated in Figure 1. As shown in Figure 1A, compared with CK, the soil organic matter (OM) content of the treatment group with organic fertilizer applied was significantly increased (p < 0.05), with an increase of 33.35% ~ 47.86%, and the CF group exhibited the highest OM value of 36.27 g/kg. This indicates that the application of organic fertilizer replacing part of the chemical fertilizer could notably enhance the content of soil OM. The soil-available phosphorus (AP) content in the CF, EF and PF groups was 70.84 g/kg, 62.89 g/kg, and 79.71 g/kg, respectively, which were significantly higher than those in the CK and FF groups (Figure 1B). This suggests that pig manure, chicken manure, and vermicompost significantly boost soil AP levels more than formula fertilizers. The soil-available potassium (AK) content in all treatment groups decreased significantly, which were FF, 63.0 g/kg, CF, 58.0 g/kg, and EF, 57.7 g/kg, respectively (Figure 1C). Compared with the FF group, the soil AK content in the PF group increased to 83.0 g/kg, indicating that the substitution of pig manure organic fertilizer improves the soil AK content and fertility environment, and also fully demonstrated that the effects of organic fertilizer from different sources on increasing AK content were different.

3.1.2. Changes in Heavy Metals and Antibiotic Concentrations

The total soil contents of Pb, Cr, Cd, Cu and Zn for different fertilization treatments are shown in Figure 2A. Compared to CK, the soil Pb contents of CM, PM and EM treatments all showed a decrease, and the Pb content of EM was reduced by 12.2% compared to FF, indicating that the Pb content in EM was reduced most obviously. For the Cd content, all treatments except PM showed a decrease compared to CK, though the reduction was not significant, in which EM had the lowest soil Cd content of 0.18 mg/kg, which may be due to the long-term rainfall part of the heavy metals with the surface runoff migration. This indicates that the application of organic fertilizers of chicken manure and vermicompost have not yet posed a risk of Cd contamination in the soil. And compared to CK, the soil Cr content of CM and EM treatments decreased by 1.5%~19.5%, and the effect of EM on the reduction in Cr content was more significant. The results of soil Cu and Zn content show that the Cu and Zn content increased significantly in PM compared to CK by 40.7% and 20.3%, respectively, whereas the soil Cu and Zn contents were lower in EM among all organic fertilizer application groups, at 9.34 mg/kg and 59.81 mg/kg, respectively, indicating that vermicompost organic fertilizer does not increase the accumulation of Cu and Zn.
Antibiotic residues in agricultural soils under different fertilizer application methods are shown in Figure 2B. The content of ENR in farmland soil increased following various fertilization treatments, and the differences between the organic fertilizer application treatment groups and the CK treatment were significant. Specifically, the CM, PM, and EM treatments increased ENR levels by 0.9, 6.2, and 4.3 times, respectively, indicating that the application of organic fertilizers introduces ENR into the soil environment to a certain degree and that organic fertilizers of pig manure > organic fertilizers of earthworm manure > organic fertilizers of chicken manure. Additionally, CIP and TET were detected only in CM and PM treatments, with concentrations of 1.67 μg/kg and 1.92 μg/kg for CIP, and 0.83 μg/kg and 1.08 μg/kg for TET, respectively, which indicates that chicken manure organic fertilizers application was the main cause of accumulation of CIP and TET in the soil, followed by pig manure organic fertilizers. And the order of the content of CHL in the soil of each treatment was PM > EM > CK > FF > CM, among which the lowest value of CHL was 0.31 μg/kg in the application of chicken manure organic fertilizer. The above results indicate that organic fertilizers with chemical fertilizers increase the risk of antibiotic accumulation in the soil, and that different organic fertilizers are associated with varying types of antibiotics.

3.2. Bacterial Community Profiles in Reddish Soil with Different Organic Fertilizers

The number of OTUs of bacteria in the treatment group in soil is shown in Figure 3A. The OTUs shared by the five groups totaled 1000, accounting for a low proportion of the total OTUs in each sample. The OTUs specific to the CK, FF, CF, EF, and PF groups were 2135, 1754, 1992, 1779, and 2163, respectively. The results showed that the bacterial community structure in soil under different organic fertilizers exhibited both similarities and specificities. Among these, the PF group had the largest number of unique OTUs, suggesting that this sample contained a greater diversity of unique microbial species. The results showed that the application of organic fertilizer changed the composition of microbial community structure in the soil.
This study found that organic fertilizer application had a significant effect on the composition and diversity of bacterial communities in red soil (Figure 3B,C). Crenarchaeota, Proteobacteria, Chloroflexi, Actinobacteria and Acidobacteriota were the dominant phyla, with relative abundances of 8.64–16.95%, 19.98–25.75%, 4.53–11.21%, 2.05–7.91%, and 8.32–9.78%, respectively. The relative abundances of Crenarchaeota, Actinobacteria and Chloroflexi in the treatment groups (EF, CF, PF) were significantly higher than that in CK (p < 0.05), while the relative abundances of Proteobacteria and Acidobacteriota were significantly reduced. Notably, the relative abundance of Gemmatimonadetes in EF was significantly higher than that of the control group, which may be due to the fact that vermicompost contains specific substances that can increase the abundance of these bacteria. Examination at the genus level indicated that Candidatus-Nitrosotalea, Methanosaeta, Rhodanobacter, MND1 and Gemmatimonas were the dominant genera in the soil, with relative abundances were 3.45–14.74%, 0.21–6.59%, 0.32–2.91%, 2.11–3.42%, and 0.28–2.43%, respectively. Compared with CK, the relative abundances of Candidatus-Nitrosotalea, Rhodanobacter and Gemmatimonas increased in fertilization treatment groups, and the relative abundance of Methanosaeta decreased significantly. Different types of fertilizer application significantly affected the relative abundance of Gemmatimonas, which increased in FF and EF but decreased in CF and PF. The alpha diversity indices of CK, FF, EF, CF, and PF are shown in Figure 4. There was a reduction in the Good coverage index, Pielou-e index and Simpson index in the other four groups compare to the control group. In addition, the Chao1, observed species and Shannon index of PF were increased. Notably, the Pielou-e index and Shannon index of EF were significantly lower than those of the control group.

3.3. Effects of Different Organic Fertilizers on Fungi Community Structure and Function in Reddish Soil

A total of 5641 OTUs were identified, of which 1152, 1148, 1049, 1093 and 1199 were identified by CK, FF, CF, PF and EF, respectively (Figure 5A). These numbers account for 20.42%, 20.35%, 17.77%, 18.59% and 21.26% of the total OTUs. The number of common fungal OTUs accounted for 4.22%, and the overlapping proportion of fungal OTUs among CF, PF and EF treatment group was 5.73%. The result showed that the EF treatment had the highest number of OTUs, reaching 638, followed by the FF treatment group with 544. The number of OTUs in the CF treatment group was at least 456, indicating that fertilization treatment had an effect on the fungal structure in the soil. Vermicompost and chicken manure improved the specificity of fungi in the soil, whereas pig manure and chicken manure reduced the specificity of fungi in the soil, with chicken manure having the most significant effect.
Based on the analysis of the fungal community under different organic fertilization, the results showed that the dominant fungal phyla in all treatments were essentially the same, with Ascomycota, Basidiomycota, Rozellomycota, Glomeromycota and Chytridiomycota being the prominent ones (Figure 5B). Ascomycota was the most dominant phylum in the soil fungal community of FF, CF, PF and EF, with average relative abundances of 44.82%, 40.61%, 41.18% and 46.24%, respectively. Compared with CK (33.06%), the application of formula fertilizer and manure significantly increased the relative abundance of Ascomycota. At the same time, the proportion of Basidiomycota in each treatment was relatively high, which were PF (37.92%), CF (32.79%), FF (28.04%), CK (23.09%), and EF (9.91%). At the genus level, the composition of fungal communities in each group of soil samples was significantly different (Figure 5C). There were 18, 20, 20, 20, 20 and 19 dominant genera of fungi in the sample soils, respectively. The sum of their relative abundances was higher than 40%, which were FF (57.23%), CF (54.23%), PF (62.94%), EF (40.74%) and CK (44.65%), respectively. Unidentified fungal genera also accounted for a considerable proportion, with Marasmiellus and Conioscypha having the highest proportions in CK treatment, with relative abundances of 14.42% and 5.79%, respectively. Compared with CK, the relative abundance of Marasmiellus in the other treatments was very low, which may be due to the effect of manure application on the bacteria activity or competition between microflora, resulting in the decreased relative abundance. Auriculariales_gen_Incertae_sedis and Deconica had the highest proportions in PF and CF samples, with relative abundances of 17.43%, 16.09%, 15.69%, and 13.14%, respectively. Figure 6 shows the alpha diversity index of fungal communities under different organic fertilizer treatments. The Chao1 index and observed species index of FF, PF, CF and EF treatments were lower than those of the basal soil samples, and the Good coverage index, Pielou-e index, Shannon index and Simpson index were higher than those of the basal soil samples.

3.4. Mechanisms of Organic Fertilizer Regulation of Soil Nutrients, Pollutants and Microbial Community Structure

3.4.1. Relationships between Soil Nutrients, Pollutants and the Role of Bacterial Communities

Redundancy analyses (RDA) were performed between the top 10 bacterial phylum level species and nutrients (organic matter: OM, available phosphorus: AP, available potassium: AK, ammonium nitrogen: NH4+-N, ammonium nitrogen: NO3−-N), and pollutants (lead: Pb, chromium: Cr, cadmium: Cd, copper: Cu, Zinc: Zn, enrofloxacin: ENR, ciprofloxacin: CIP, tetracycline hydrochloride: TET, chrysin hydrochloride: CHL) (Figure 7A). The analysis revealed that Crenarchaeota, Proteobacteria, Actinobacteria, Acidobacteriota, and Gemmatimonadetes showed significant positive correlation with AP and NO3−-N, while Chloroflexi, unidentified_bacteria had significant positive correlation with AK. Additionally, Chloroflexi, unidentified_bacteria and Acidobacteriota showed significant positive correlations with NH4+-N. Proteobacteria, Actinobacteria, Acidobacteriota, Gemmatimonadetes were significantly positively correlated with Cr, Pb, TET, CIP, ENR, whereas unidentified_bacteria showed significant positive correlations with Cu and Zn. Meanwhile Halobacterota, Myxococcota were positively correlated with Cd, while Crenarchaeota, Actinobacteria, Acidobacteriota, Gemmatimonadetes were significantly negatively correlated with CHL. The results of this study revealed complex and diverse relationships between soil nutrients, pollutants and bacterial community roles, offering new strategies for pollution regulation.
To further clarify the effects of bacterial communities with nutrients (OM, AP, AK, NH4+-N, NO3−-N) and pollution (Pb, Cr, Cd, Cu, Zn, ENR, CIP, CHL, and TET), we performed correlation analyses between bacteria and nutrients, and pollutants at the genus level, as shown in Figure 7B. The heat map results reveal that Methanosaeta, Anaeromyxobacter, Geothrix, and Methanosarcina are negatively correlated with Pb, CHL, OM, and pH, and all of these, except Geothrix, have the most significant correlation with pH, though Geothrix shows a more significant correlation with Pb and OM. While Gemmatimonas, Ellin6067, Candidatus_Solibacter, Candidatus_Koribacter, Oryzihumus, Sphingomonas, Pseudolabrys, Mycobacterium showed positive correlations with Pb, Cr, CHL, OM, and pH, of which all being significantly positively correlated with pH except Ellin6067, Oryzihumus, Sphingomonas. Meanwhile, Candidatus_Solibacter, Candidatus_Koribacter, Pseudolabrys, and Mycobacterium were also stronger correlations with Pb, indicating that these key microorganisms can effectively regulate changes in heavy metals and nutrients in soil.

3.4.2. Correlation among Fungi with Physicochemical Factors and Pollutions

RDA were performed between the top 10 fungal phylum level species and nutrients (OM, AP, AK, NH4+-N, NO3−-N), and pollutants (Pb, Cr, Cd, Cu, Zn, ENR, CIP, CHL, and TET) (Figure 8A). The RDA results showed that Entorrhizomycota, Glomeromycota, Kickxellomycota and EC, ENR, Cu were significantly positively correlated; while Basidiomycota was significantly positively correlated with Cd, CIP, TET, Cr, suggesting that the strain can effectively regulate pollutant concentrations. Mortierellomycota showed a significant positive correlation with OM, pH, and Pb, with the highest correlation with OM. Chytridiomycota showed a significant positive correlation with CHL and Pb, indicating that the abundance of this strain directly affects the concentrations of CHL and Pb in soil. Rozellomycota, Fungi_phy_Incertae_sedis, and Mucoromycota showed a significant positive correlation with NH4+-N, suggesting that three strains can influence the processes of nitrogen transformation.
In order to further clarify the effects of fungi communities with nutrients and pollution, we performed correlation analyses between fungi and nutrients (OM, AP, AK, NH4+-N, NO3−-N), and pollutants (Pb, Cr, Cd, Cu, Zn, ENR, CIP, CHL, and TET) at the genus level, as shown in Figure 8B. The thermogram results indicate that Psilocybe is positively correlated with Pb, Cr, Cu, Zn, AK, NO3−-N, pH, and EC, of which the most significant correlation was observed with Pb, while it is negatively correlated with Cd, CHL, and NH4+-N. Marasmiellus showed a significant negative correlation with ENR and AP, while Lasiobolus showed a positive correlation with all indicators except Pb, CHL, OM and NH4+-N, with the most significant correlation with AP. Botryotrichum showed a significant positive correlation with Pb and OM, suggesting that it might be a heavy metal Pb-carrying strain, with levels changing in accordance with its abundance, and simultaneously affecting the degradation of OM. Entoloma showed a significant negative correlation with Cd, indicating that this strain can effectively reduce the content of heavy metal Cd in soil. Both Ascodesmis and Curvularia showed significant positive correlations with Cu, Zn, AK, and EC, and significant negative correlations with CHL, suggesting that these strains might have a simultaneous regulatory effect on heavy metals, nutrients, and antibiotics. Oehlia showed a significant negative correlation with Pb and OM, suggesting that this strain might be a key bacterium for Pb passivation and regulation of soil OM content simultaneously. Pseudeurotium showed a significant positive correlation with ENR but a significant negative correlation with OM, indicating that this strain reduces the ENR of the antibiotic without affecting the OM content.

4. Discussion

Compost products, as a type of organic fertilizer, significantly enhance soil quality by affecting its physical, chemical and biological properties. Organic fertilizer applied to the soil can effectively improve soil permeability, increase soil pore space, and help the formation of soil granular structure, thereby improving soil physical properties. Additionally, compost products are generally alkaline and can be used to neutralize soil acidity. Proper application of organic fertilizers can provide elements that promote plant growth, leading to improved crop yield and quality [49]. Animal manure, which is rich in nutrients, further promotes plant growth and contributes high crop yields. Studies have shown that the application of organic fertilizers can increase the yield of crops such as maize [50], potatoes [51] and tomatoes [52]. Furthermore, studies have shown that because pig manure contains nitrogen, phosphorus, potassium and OM, the application of pig manure organic fertilizer can increase soil nutrient content, pH value and available water [41]. In this study, the application of 15% organic fertilizer increased the contents of OM, AP and AK in the soil, with pig manure proving to be the most effective.
Heavy metals in organic fertilizers from livestock and poultry manure are known to mainly include Cu, Zn, Pb, Cd and Cr. Studies have shown that application of organic manure from swine manure significantly increases the biomass of peanut (Arachis hypogaea L.) crop, but also raise the levels of Cu, Zn and Cd contamination in the soil [53]. Therefore, inappropriate or excessive application of organic manure carries the risk of exacerbating heavy metal contamination in agricultural soils [54,55]. In addition, the concentration of Cu and Zn in crops is closely related to the amount of extractable Cu and Zn in the soil. In this study, there was no significant accumulation of heavy metals in the soil after the application of different types of organic fertilizers, suggesting that the short-term application of organic fertilizers instead of chemical fertilizers has not yet posed a risk of heavy metals (Cu, Zn, Pb, Cd and Cr). Furthermore, organic fertilizers can effectively change the diversity and abundance of soil microorganisms, thus affecting the structure and spatial distribution of soil microbial communities [56,57,58,59]. And different kinds of organic fertilizers have varying effects on soil nutrients and crop growth [60]. Simultaneously, the application of different organic fertilizers also influences the activity of enzymes involved in biochemical reactions and material metabolism processes in the soil, thus affecting the number and composition of the dominant microbiota [61]. For example, the application of 10% compost products significantly increased soil enzyme activity and bacterial community composition diversity [62]. In this study, the diversity of soil bacterial communities decreased after the application of organic fertilizer, except for the PF group. The order of bacterial community diversity was PF > CF > EF > FF, that is the soil bacterial community diversity was higher in the organic fertilizer treatment than in the formulated chemical fertilizer treatment. There were differences in fungal and bacterial community diversity, where PF and CF decreased after organic fertilizer application, but EF and FF groups were elevated. The order of fungal community diversity was EF > FF > PF > CF.
In this study, the pre-treatment of organic manure is enhanced to improve the harmlessness of the process. This treatment reduces the concentration of pollutants when the manure is returned to the field, thereby minimizing the environmental risks associated with livestock manure at the source. Therefore, we recommend farmers to use vermicompost as an alternative to chemical fertilizers in agriculture. The type of crop grown also plays a crucial role in the pollution impact of livestock manure returned to the field. Some crops that are resistant or enriched can significantly affect pollutant concentrations, thereby influencing the risk level of manure in the soil environment. Additionally, a long-term fixed experiment is needed to further validate the effects of organic fertilizer application on soil biological community structure and the stability of functional microorganisms after application.

5. Conclusions

In this study, we investigated the impact of organic fertilizer on the soil microbial community and its effect on the ecological risk of farmland soil. Soil nutrients are influenced by the type of fertilizer applied, and organic fertilizers, when used to replace chemical fertilizers, can effectively increase OM, AP, and AK levels in the soil. The application of organic fertilizers significantly impacts the indigenous soil microenvironment, modulating the species and abundance of both commensal and heterogeneous soil microorganisms. The vermicompost treatment resulted in significantly lower heavy metal concentrations (Cu, Zn, Pb, Cr and Cd) in the soil after planting compared to the other treatment groups, indicating that short-term application of vermicompost does not lead to heavy metal accumulation. The antibiotic concentrations in the soil showed an increasing trend after the application of 15% replacement of vermicompost, with more significant increases in the ENR and CHL concentrations. Overall, the application of organic fertilizers affects the microbial community structure of red soils in South China and enhances soil nutrients in agricultural fields. We hope that this study improves understanding of how the organic fertilizer returned to the field ecological regulates soil environment.

Author Contributions

Data curation, Z.H. and C.W.; formal analysis, Q.Z.; funding acquisition, Q.S., Y.L. and H.X.; investigation, Z.H.; methodology, Q.Z., Z.H. and C.W.; project administration, H.X.; resources, Q.S.; supervision, Y.L. and H.X.; writing—original draft, Q.S. and Q.Z.; writing—review and editing, Q.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Natural Science Foundation of Guangdong Province (No. 2023A1515010593), the Open Competition Program of Ten Major Directions of Agricultural Science and Technology Innovation for the 14th Five-Year Plan of Guangdong Province (2022SDZG08) and the earmarked fund for CARS-14, the China Postdoctoral Science Foundation (No. 2023M731141).

Data Availability Statement

The data presented in this study are available on request from the corresponding author on reasonable request.

Acknowledgments

Thank you to the Key Laboratory of Arable Land Conservation (South China) and Guangdong Province Key Laboratory for Land Use and Consolidation for providing experimental conditions. Thank you to Yongtao Li and Hui-Juan Xu for providing financial support for the experiment.

Conflicts of Interest

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this paper.

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Agronomy 14 02150 g001
Figure 1. Changes in the organic matter (A), available phosphorus (B) and available potassium (C) in different fertilizer treatments. Results are the mean of three replicates and error bars indicate standard deviation. Different letters meant there was significant difference among groups (p < 0.05). CK, FF, EF, CF and PF mean soil with unfertilized, formula fertilizer, earthworm manure, chicken manure and pig manure.
Figure 1. Changes in the organic matter (A), available phosphorus (B) and available potassium (C) in different fertilizer treatments. Results are the mean of three replicates and error bars indicate standard deviation. Different letters meant there was significant difference among groups (p < 0.05). CK, FF, EF, CF and PF mean soil with unfertilized, formula fertilizer, earthworm manure, chicken manure and pig manure.
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Figure 2. Effects of different fertilization methods on heavy metal contents (A) and antibiotic content (B) in soil.
Figure 2. Effects of different fertilization methods on heavy metal contents (A) and antibiotic content (B) in soil.
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Figure 3. Dynamic changes in bacterial community structure: Venn diagram (A), the phyla level (B) and the genera level (C) in different fertilizer treatments.
Figure 3. Dynamic changes in bacterial community structure: Venn diagram (A), the phyla level (B) and the genera level (C) in different fertilizer treatments.
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Figure 4. Analysis of α diversity of bacterial community in soil under different fertilization treatments.
Figure 4. Analysis of α diversity of bacterial community in soil under different fertilization treatments.
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Figure 5. Dynamic changes in fungal community structure: Venn diagram (A), the phyla level (B) and the genera level (C) in different fertilizer treatments.
Figure 5. Dynamic changes in fungal community structure: Venn diagram (A), the phyla level (B) and the genera level (C) in different fertilizer treatments.
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Figure 6. Analysis of α diversity of fungal community in soil under different fertilization treatments.
Figure 6. Analysis of α diversity of fungal community in soil under different fertilization treatments.
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Figure 7. Redundancy analysis ((A): phylum level) and heatmap ((B): genus level) of the relationship between nutrient parameters and pollutant and bacterial community.
Figure 7. Redundancy analysis ((A): phylum level) and heatmap ((B): genus level) of the relationship between nutrient parameters and pollutant and bacterial community.
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Figure 8. Redundancy analysis ((A): phylum level) and heatmap ((B): genus level) of the relationship between nutrient parameters and pollutant and fungal community.
Figure 8. Redundancy analysis ((A): phylum level) and heatmap ((B): genus level) of the relationship between nutrient parameters and pollutant and fungal community.
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Table 1. Fertilizer type and amount of different treatments.
Table 1. Fertilizer type and amount of different treatments.
TypeBased Fertilizer (g)Supplement Fertilizer (g)
Organic FertilizerUreaSuperpho-
Sphate		Potassium ChlorideUreaPotassium Chloride
CK000000
FF03531955142823332
CM26,0003001955142700332
PM26,0003001955142700332
EM26,0003001955142700332
Note: (Based on test plot size (35 m2)).
Table 2. The basic physicochemical properties of organic fertilizer.
Table 2. The basic physicochemical properties of organic fertilizer.
Organic FertilizerNutrient Content (g/kg)Heavy Metals Content (mg/kg)Antibiotic Content (μg/kg)
Organic MatterTotal NitrogeTotal PhosphorusTotal PotassiumCuZnPbCdCrEnrofloxacinCiprofloxacinChlorotettracyclineTetracycline
Chicken manure101.524.16.129.382.3167.215.20.318.166.17.521.35.8
Pig manure283.9 17.219.724.272.3127.313.70.49.710.94.047.45.0
Earthworm manure266.613.27.167.855.386.69.20.37.80.3-3.0-
Note: “-” Antibiotic content is not detected.
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Sun, Q.; Zhang, Q.; Huang, Z.; Wei, C.; Li, Y.; Xu, H. Effect of Organic Fertilizer Application on Microbial Community Regulation and Pollutant Accumulation in Typical Red Soil in South China. Agronomy 2024, 14, 2150. https://doi.org/10.3390/agronomy14092150

AMA Style

Sun Q, Zhang Q, Huang Z, Wei C, Li Y, Xu H. Effect of Organic Fertilizer Application on Microbial Community Regulation and Pollutant Accumulation in Typical Red Soil in South China. Agronomy. 2024; 14(9):2150. https://doi.org/10.3390/agronomy14092150

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Sun, Qinghong, Qiao Zhang, Zhijie Huang, Chang Wei, Yongtao Li, and Huijuan Xu. 2024. "Effect of Organic Fertilizer Application on Microbial Community Regulation and Pollutant Accumulation in Typical Red Soil in South China" Agronomy 14, no. 9: 2150. https://doi.org/10.3390/agronomy14092150

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