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Article

Enhancement of Rhizoma Atractylodis Quality, Soil Nutrients, and Microbial Characters of Vermicompost Preparations from Spent Mushroom and Cow Dung

by
Baoyi Sun
1,2,†,
Shuqiang Wang
1,2,†,
Ying Zhang
1,
Bin Chen
1,
Pengcheng Li
1,2,
Xianying Zhang
1,
Yonghuan Wang
3,
Mingyi Zhao
1,
Yulan Zhang
1,4,5,6,* and
Hongtu Xie
1,4,5,6,*
1
CAS Key Laboratory of Forest Ecology and Silviculture, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
2
University of Chinese Academy of Sciences, Beijing 100049, China
3
Liaoning Agricultural Development Service Center, Shenyang 110034, China
4
National Field Observation and Research Station of Shenyang Agro-Ecosystems, Shenyang 110107, China
5
Key Laboratory of Terrestrial Ecosystem Carbon Neutralization, Shenyang 110016, China
6
Key Laboratory of Conservation Tillage and Ecological Agriculture, Shenyang 110016, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to the work.
Agronomy 2024, 14(7), 1384; https://doi.org/10.3390/agronomy14071384
Submission received: 29 May 2024 / Revised: 24 June 2024 / Accepted: 25 June 2024 / Published: 27 June 2024
(This article belongs to the Section Agricultural Biosystem and Biological Engineering)
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Abstract

:
Organic fertilizers produced from agricultural waste materials using earthworms have many advantages. The impact of vermicompost bio-organic fertilizer (VcF) prepared from waste mushroom bran on the quality of Chinese herbal medicine and soil health deserves attention. We conducted a field experiment to explore the quality of Rhizoma atractylodis and soil, using chemical fertilizer and VcF at dosages of 30 t·ha−1 and 40 t·ha−1. The results demonstrated that VcF significantly increased the contents of atractylenolide II, β-eudesmol, atractylenol, and atractylenolone by 34%, 175%, 72%, and 24%, respectively, along with a 70% increase in yield compared to the control. VcF significantly increased the available phosphorus content and the activity of the soil enzymes (α-Galactosidase, β-Galactosidase, and peroxidase), while reducing the nitrate nitrogen content. The addition of vermicompost did not change the soil bacterial diversity, while it significantly increased the soil fungal diversity. VcF improved the soil fungal diversity and significantly enhanced the relative abundance of the bacterial phylum Actinobacteriota and WPS-2, as well as the fungal phylum Ascomycota. Vermicompost significantly increased the relative abundance of bacteria phylum Actinobacteriota and WPS-2, as well as the fungi phylum Ascomycota. Actinobacteria mainly participate in the decomposition of detritus and the heterotrophic nutrient cycle. A Principal Coordinates Analysis of the soil bacterial and fungi communities suggested a significant impact of vermicompost application on the community structure of the soil bacteria. Conversely, no significant variance was detected in the bacterial community composition across the two levels of vermicompost. This study contributes to the enhancement of fertilization strategies for Atractylodes macrocephala, broadens the application scope of vermicompost, and advances the growth of organic agriculture.

1. Introduction

The recycling of waste resources can be achieved by treating agricultural residual edible fungus bran through composting technology [1,2]. The application of organic fertilizers mitigates the adverse effects of agriculture on soil ecosystems and provides healthier and better-quality agricultural products, thereby promoting sustainable and environmentally friendly agriculture [3].
Vermicomposting technology has more advantages than conventional composting due to the better quality of the compost products [4]. The nutrients in vermicompost vary depending on the raw materials. It is the by-product of mushroom cultivation. It refers to the leftover culture medium that remains after edible mushrooms have been harvested. Approximately 15 million tons of discarded edible mushroom bran are produced annually in China, whose fertilizer utilization is of great significance for resource reuse and environmental protection [2,5]. Vermicompost prepared from edible mushroom bran is rich in organic matter, nitrogen, phosphorus, potassium, humic acid, amino acids, numerous diverse microorganisms, and other beneficial substances [4].
The use of vermicompost can be found in various agricultural practices, including the cultivation of vegetables, crops, fruits, and as substrates for seedlings [6]. Researchers have paid close attention to the effects of vermicompost application on seed germination rate, crop yield, crop quality, and soil quality [7,8,9,10,11,12]. Vermicompost has been used as fertilizer or soil conditioner for cultivating traditional Chinese medicine plants, improving the yield of chicory [13], saffron [14], and enhancing the quality of garlic [15]. Vermicompost prepared from mushroom bran and pig manure increased the germination rate of corn seeds [16]. The application of vermicompost significantly increased the yield of crops such as tomatoes, watermelons, potatoes, goji berries, strawberries, chili peppers, marigold, tobacco seedlings, and cucumbers [17,18,19]. Many studies have focused on the changes in quality indicators such as vitamins, soluble sugars, and soluble proteins in crops [20]. One study found that vermicompost increased the contents of soluble solids, soluble sugars, and vitamin C in strawberries [21].
Soil nutrient cycling and availability were positively affected by vermicompost. Vermicompost demonstrates a greater efficacy compared to other soil amendments in enhancing soil fertility, potentially attributed to its superior drainage, water retention, and fertilizer supply capabilities [22]. A previous study revealed that vermicompost enhanced the soil nutrient levels, porosity, aeration, drainage, permeability, enzymatic catalytic activities, abundance of microorganisms, and the structure of microorganisms, thereby establishing a more conducive environment for plant root growth [23,24]. Vermicompost, serving as a bio-organic fertilizer, enhances plant growth through diverse mechanisms such as growth regulators, hormones, disease-resistant strains, and the suppression of plant pathogens via antibiotics and bacteriocins. It also enhances nitrogen fixation, the mineralization of organic phosphorus, and other mineral absorption with digestive enzymes, indoleacetic acid, and more [22,25]. The enhancement of soil nutrient activation was more effectively facilitated in soil treated with vermicompost, which was partly due to beneficial substances such as amino acids, indole-3-acetic acid, and digestive enzymes.
Essential nutrients for plant growth and microbial activity can be acquired from vermicompost, which helps to improve the community structure and biodiversity of the soil [26]. Vermicompost possesses a substantial particle surface area, offering an extensive site for microbial activities [27]. It was documented that the application of vermicompost resulted in an increase in the Chao1 and Shannon indices of the soil bacterial community [1]. Additionally, there was a significant increase in the absolute abundance of soil fungi. The utilization of vermicompost also suppressed the proliferation of certain parasitic fungi, such as Botrytis cinerea, known for inducing gray mold [28]. Disease-resistant strains have been shown to enhance soil microbial growth and increase microbial activity [23]. The impact of vermicompost on soil microbiological characteristics is dependent on various factors, including the composition and amount of vermicompost, the crop type, soil composition, and soil properties [6].
The plant Atractylodes chinensis (DC.) Koidz is extensively utilized in traditional Chinese herbal medicines and the health product industries [29]. The presence and concentration of active compounds in the rhizome, such as Rhizoma atractylodisin, β-eudesmol, and sesquiterpenes, among others, serve as indicators of the plant’s quality [30]. Rhizoma atractylodisin is the main active compound found in Atractylodes macrocephala and has a range of pharmacological effects, including anti-inflammatory, anti-tumor, antibacterial, antiviral, hypoglycemic, and diuretic properties [31,32]. Rhizoma atractylodisinone also exhibits similar effects, along with hepatoprotective and anti-aging properties. Atractylodes macrocephala endolipid II has anti-inflammatory and anti-tumor effects, helps to regulate gastrointestinal function, and enhances nutrient absorption. The volatile oil from Atractylodes macrocephala, primarily composed of β-eudesmol, shows promise in treating pediatric rickets [33]. The optimal amount of vermicompost organic fertilizer for enhancing the yield and quality of traditional Chinese medicinal herbs is currently unknown, prompting the need for this experiment. This study aimed to assess the effects of vermicompost application on soil properties, as well as the yield and quality of Atractylodes lancea (Thunb.) through field experiments.

2. Materials and Methods

2.1. Experimental Design

The experiment was conducted in Xiuyan county, Anshan City, Liaoning Province (E: 123.671809, N: 40.507569). The study area is defined by a temperate humid monsoon climate abundant in moisture and light. The annual average rainfall in the study region ranges from 750 mm to 1000 mm, with the majority falling between July and September, representing 73.5∼80.2% of the total annual precipitation. The annual average temperature is 8 °C. The study area is predominantly characterized by low mountains, which cover approximately 78% of the total area. The soil in the study area is classified as brown loam soil (FAO-UNESCO system).
The present experiment was carried out in the field. The test variety of Atractylodes chinensis (DC.) [34]. Koidz used in this study is commonly referred as “North Rhizoma atractylodis”. We transplanted the roots of two-year-old Rhizoma Atractylodis with the objective of obtaining roots from three-year-old Rhizoma Atractylodis. In accordance with local agricultural practices, Atractylodes was sown in May and subsequently reaped during October.
The experiment implemented three distinct treatments, with each treatment being replicated three times. Each plot was arranged in dimensions of 50 m × 0.5 m, with a 0.5 m wide blank area established between the plots to reduce the impact of water and nutrient movement. Three treatments were established as CK (chemical fertilizer), VcF (low vermicompost dosage of 30 t·ha−1), and VcF2 (high vermicompost dosage of 40 t·ha−1). We previously employed a low vermicompost dose of 30 t·ha−1 to improve the plant yield. Therefore, we established VcF and VcF2 treatments.
Farmers typically apply chemical fertilizers exclusively during the planting of Rhizoma atractylodis. The chemical compound fertilizer (12-16-16) used in the experiment was purchased from the market. It contained 12% nitrogen (N), 16% phosphorus oxide (P2O5), and 16% potassium oxide (K2O) (potassium sulfate). All agronomic practices, including weeding and pest control, adhered to local customs. Vermicompost bio-organic fertilizer was prepared from a combination of edible mushroom bran and cow dung in a 2:8 ratio using earthworms. We obtained the edible mushroom bran and cow dung materials from farmers. We left the cow dung to naturally and ecologically degrade over 7 days and used crushed edible mushroom bran as a pre-treatment. We mixed the mushroom bran with cow dung and built several feeding beds for breeding the earthworms. We obtained vermicompost bio-organic fertilizers after collecting the earthworms.

2.2. Plant and Soil Sampling

In 2021, during the ripening season in October, three randomly chosen sampling areas were selected per replicate block to gather Rhizoma Atractylodis root. We only obtained yield data for CK and VcF because farmers removed the roots in the VcF2-treated plots. We cleaned the root samples and allowed them to naturally dry in a ventilated area. We collected samples of each duplicate together due to carelessness and weighed them with an electronic balance. The weight was converted to kg·ha−1. The plant samples were pulverized and homogenized.
We collected five soil cores randomly (0–20 cm) in each replicated block using a soil auger (20 cm in diameter), removed debris, and mixed them into one soil sample. After being transported back to the laboratory with dry ice, each soil sample was divided into three parts. The first sample was stored at −80 °C for the DNA extraction of soil microorganisms. The second sample was sieved through a 2 mm mesh and stored at 4 °C for determining the soil enzyme activity. The other part was air-dried and sieved through a 2 mm mesh for a soil properties analysis.

2.3. Plant Analysis

The quality parameters of Rhizoma Atractylodis were assessed. High-performance liquid chromatography (HPLC) was employed utilizing a one-measure-multiple-measure approach to quantify the concentrations of atractyloxin, β-eudesmol, atractylenolide I, and atractylenolide II [35]. The soil pH was determined by measuring a 1:2.5 soil/water suspension using a digital pH meter (pH 700 Bench Meter, Eutech Instruments, Singapore).

2.4. Soil Physiochemical and Enzymatic Properties Analysis

The ring knife method was utilized to ascertain the bulk density of the soil. Soil organic C (SOC) was quantified using the K2Cr2O7 solution oxidation method [36]. Soil total C (TC) and total N (TN) were quantified by combusting dried subsamples (sieved through a 0.16 mm mesh) using an automatic elemental analyzer (Analyzer Vario MICRO cube, Elementar, Langenselbold, Germany). Soil total phosphorus (TP) was assessed through perchloric acid HClO4 digestion [37]. Soil total potassium (TK) and available potassium (AK) were measured using the flame photometer method [38]. The concentration of soil nitrate nitrogen was determined utilizing the sulphamic acid UV spectrophotometric method [39]. The indophenol blue colorimetric method was employed for quantifying the soil ammonium nitrogen [40]. The content of soil available phosphorus (AP) was evaluated through extraction using a 0.5 mol·L−1 NaHCO3 solution and detected by spectrophotometry.
We selected several soil enzymes involved in the C-cycling process. These enzymes are closely associated with the biogeochemical transformation process in soil and are utilized as representative indicators for the status of soil microbial nutrients [41,42,43]. Soil carbon-cycling enzymes comprise α-D-Glucosidase (AG, EC. 3.2.1.20), β-D-Glucosidase (BG, EC. 3.2.1.21), α-Galactosidase (AGal, EC. 3.2.1.22), β-Galactosidase (BGal, EC. 3.2.1.23), Xylanase (Xyl, EC. 3.2.1.8), N-acetyl-D-aminoGlucosidase (NAG, EC. 3.2.1.30), phenol oxidase (EC. 1.10.3.2), and peroxidase (EC. 1.11.1.7). The activities of soil AG, BG, AGal, BGal, Xyl, and NAG were determined using fluorogenic substrates [44]. Specially, (I) AG was assessed with 4–methylumbelliferyl-α-D-glucopyranoside, (II) BG was assessed with 4-methylumbelliferyl-β-D-glucopyranoside, (III) Agal was assessed with p-nitrophenylgalactoside, (IV) BGal was assessed with p-nitrophenyl-β-D-galactoside, (V) Xylanase was assessed with Xylan, and (VII) N-acetyl-D-aminoGlucosidase was determined using p-nitrophenyl-N-acetyl-D-aminoglucoside as the substrate. Soil phenol oxidase activity was assessed using the L-DOPA method, while soil peroxidase activity was determined using the gallic acid method. Soil dehydrogenase (DHA), an intracellular enzyme classified as EC 1.1.1), was selected as a key indicator of soil microbial activity in the present study [45].

2.5. DNA Extraction, Quantifications of Gene Abundance, and High-Throughput Sequencing

Following the manufacturer’s protocol, we utilized the Power Soil® DNA Isolation Kit (MoBio, Hanoi, Vietnam) to extract the total genomic DNA from 0.5 g of frozen soil. The quality of the total DNA was assessed utilizing the Nano Drop ND-2000 spectrophotometer manufactured by Thermo Fisher Scientific (Waltham, MA, USA). The quantification of the 16S rRNA and ITS genes was conducted using quantitative polymerase chain reaction (qPCR) on an ABI 7500 Real-Time PCR System (Applied Biosystems™, Waltham, MA, USA) in accordance with the manufacturer’s instructions. For the quantification of the total bacterial abundance using the 16S rRNA gene, a universal primer set was employed, consisting of 338F: 5′-ACTCC TAC GGG AGG CAGCAG-3′ and 518R: 5′-ATTAC CGC GGC TGC TGG-3′. In the case of ITS analysis, the primers utilized were ITS1: 5′-CTTGG TCA TTT AGA GGA AGTAA-3′ and ITS2: 5′-TGCGT TCT TCA TCG ATGC-3′ [1]. The cycling conditions consisted of an initial denaturation step at 95 °C for 30 s, followed by 40 cycles with an annealing temperature of 60 °C for 40 s. The PCR mixture was composed of 16.5 μL of Power SYBR® Green PCR Master Mix (Applied Biosystems™, Thermo Fisher Scientific Inc.), 0.8 μL of each primer, and 2 μL of the extracted DNA template. The specificity of the amplification in the reaction was validated through the generation of a melting curve. Standard curves were generated through a tenfold serial dilution of the cloned plasmid. Subsequently, the copy numbers of different genes were quantified per gram of dry soil using these standard curves. For high-throughput sequencing, the amplification protocol consisted of an initial hot start at 95 °C for 5 min, followed by 28 cycles of denaturation at 95 °C for 45 s, annealing at 55 °C for 50 s, and extension at 72 °C for 45 s. The protocol concluded with a final extension step at 72 °C for 10 min. The PCR products were purified using an Agencourt AMPure XP Kit. The sequencing was performed utilizing an MiSeq platform at Allwegene Company (Beijing, China). The sequence data were deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive under the accession number PRJNA808813.

2.6. Statistical Analyses

The normality of all data was assessed using the Shapiro–Wilk normality test. Subsequently, one-way ANOVA with Duncan’s test (p < 0.05) was conducted to detect variations in different indices using SPSS 20.0 (SPSS).
The α-diversity of soil bacteria and fungi was assessed using the “picante” package in R (version 4.1.2, http://www.r-project.org (accessed on 6 October 2023)). We computed Pearson’s correlations among the soil properties, operational taxonomic units (OTUs) of bacteria and fungi, and the relative abundances of dominant phyla and genera using the “Hmisc” package. A principal coordinate analysis (PCoA) utilizing the Bray–Curtis distance metric was conducted using the “vegan” package in R to evaluate the β-diversity. The gene β-diversity was assessed through a similarity analysis using ANOSIM, with 999 permutations. The “ggplot2” package in R was utilized for data visualization, while the visualization of phylum/genus and Spearman’s correlations was achieved using the “pheatmap” and “corrplot” packages.

3. Results

3.1. Effect of Vermicompost on the Yield and Quality of Rhizoma Atractylodis

Vermicompost (30 t·ha−1) application significantly increased the contents of Atractylodes macrocephala endolipid II by 34%, β-eudesmol by 175%, atractylodinone by 72%, and atractylodinone by 24% (Figure 1). Moreover, the application of vermicompost significantly enhanced the yield of Atractylodis.

3.2. Effect of Vermicompost Application on Soil Physicochemical Properties and Enzymes Activities

No significant differences were noted in the soil bulk density (BD), ammonium nitrogen (NH4+-N) concentration, total carbon (TC), total nitrogen (TN), total phosphorus (TP), and total potassium (TK) between the plots treated with chemical fertilizers (CK) and the plots treated with a low-dose vermicompost (VcF) or high-dose vermicompost (VcF2) (Figure 2). The application of the VcF and VcF2 treatments led to a significant increase in the soil available phosphorus (AP) content by 25% and 20%, respectively. No significant variances were detected between the VcF and VcF2 treatments. The application of VCF and VcF2 treatments led to a significant reduction in the soil nitrate nitrogen content by 52% and 54%, respectively. No significant disparities were observed in the NH4+-N indices between the two treatments, VCF and VCF2 (Figure 2).
Both the VcF and VcF2 treatments led to a significant reduction in soil α-Glucosidase activity by 58% and 46%, respectively (Figure 3). The enzymes showed a minimal response to the application of vermicompost, as evidenced by only slight variations in the activity levels of xylanase, N-acetyl-β-D-glucosaminidase, phenol oxidase, and peroxidase. Both VcF and VcF2 resulted in an increase in α-Galactosidase and β-Galactosidase activities, as well as a decrease in β-Glucosidase activity; however, these variances were not deemed statistically significant.

3.3. Effect of Vermicompost on Soil Microbial Quantity and Community Structure

Based on the observed values, the vermicompost treatments showed a tendency to enhance the absolute gene copy numbers of soil bacteria and fungi (Figure 4). The VcF treatment exhibited the highest copy numbers of 16S and ITS genes. Nevertheless, the variances among the three treatments did not demonstrate statistical significance.
After conducting sequencing analysis on the soil bacteria, it was observed that the CK, VcF, and VcF2 treatments each harbored distinct operational taxonomic units (OTUs), with 210, 121, and 126 OTUs, respectively (Figure 4). These accounted for 5.7%, 3.3%, and 3.4% of the total OTUs, respectively. The VcF and CK plots exhibited 243 shared operational taxonomic units (OTUs), while VcF2 and CK shared 238 OTUs. Additionally, the VcF and VcF2 plots shared 268 OTUs. There were no significant differences observed in the Chao1, Simpson, and Shannon indices of the sequencing results of the soil fungi, indicating that the CK, VcF, and VcF2 treatments each harbored distinct operational taxonomic units (OTUs), with 181, 229, and 226 OTUs, respectively. These OTUs accounted for 10.7%, 13.5%, and 13.4% of the total OTUs respectively. The VcF and CK plots exhibited 184 shared OTUs, while VcF2 and CK shared 282 OTUs. Additionally, the VcF and VcF2 plots collectively harbored 430 shared OTUs. The disparity in fungal composition observed between VcF and VcF2 was greater than that between VcF2 and CK, following the treatments with VcF and CK.
The VcF2 treatment significantly influenced the alpha diversity of the soil fungal community (Figure 4). The VcF2 treatment led to a notable 15% increase in the Chao1 index and a 20% increase in the Shannon index. In contrast, the use of VcF did not result in significant variations in either the Chao1 or Shannon indices. There were no statistically significant variances observed in the Simpson’s index across the three treatment groups.
The top 14 phyla of soil bacteria are shown in Figure 5. Proteobacteria, Acidobacteriota, Chloroflexi, Actinobacteriota, WPS-2, and Planctomycetota are depicted in percentage bar charts. They exhibited relative abundances ranging from 20.81% to 29.75%, 20.72% to 35.43%, 6.41% to 15.01%, 6.40% to 12.13%, 2.75% to 5.78%, and 1.16% to 1.87%.
Twenty-three of the soil bacteria genera were selected and are presented as percentage bar charts. The relative abundances of Humicola, Inocybe, and Podospora were significantly enhanced by both the vermicompost and high-dosage vermicompost treatments. The relative abundance of saprophytic bacteria in the vermicompost and dosed vermicompost treatments increased by 588% and 526% relative to the control treatment CK. Moreover, the relative abundance of Inocybe was 1.26 times higher in the vermicompost treatment and 0.82 times higher in the high-dosage vermicompost treatment compared to the control. Moreover, the relative abundance of Sclerotinia spp. increased by 5.75 and 4.49 times, respectively, in comparison to the control treatment. The relative abundance of Pseudaleuria spp. was notably enhanced through the application of vermicompost. The expression of Pseudaleuria spp. increased by 10.65-fold compared to the control treatment, whereas no significant variance was observed between the control and the vermicompost treatments. The application of a high dosage of vermicompost increased the relative abundance of Alpinaria spp. by 2.71-fold compared to the control treatment, with no significant variation observed between the vermicompost treatments and the control treatment.
The six fungal phyla with the highest relative abundance, namely Ascomycota, Basidiomycota, Mortierellomycota, Glomeromycota, Chytridiomycota, and unidentified phyla, were isolated and are displayed as percentage bars (Figure 5). The relative abundances of these fungal phyla ranged from 43% to 57%, 24.35% to 40.29%, and 24.35% to 40%, respectively. The relative abundance of Glomeromycota ranged from 43.87% to 57.42%, Chytridiomycota from 24.35% to 40.29%, and unidentified phyla from 3.91% to 5.21%.
The proportion of Actinomycetes in VcF and VcF2 increased by 43% and 33%, respectively, compared to CK. The relative abundance of the WPS-2 phylum increased by 43% and 56% in the vermicompost and spiked vermicompost treatments, respectively, compared to CK. Conversely, the relative abundance of Verrucomicrobiota in the vermicompost-treated samples decreased significantly by 37% and 35%. The relative abundance of unidentified genera of Acidobacteria (uncultured Acidobacteria bacterium) was significantly reduced by 32% in the vermicompost treatment (Figure 6). Furthermore, dosed vermicompost resulted in a significant 52% increase in the relative abundance of Burkholderia-Caballeronia-Paraburkholderia. Similarly, the VcF treatment significantly increased the relative abundance of Bradyrhizobium spp. by 73% and 59%, which is comparable to the VcF2 treatment.
The relative abundance of the Ascomycetes phylum exhibited a notable increase of 31% under the high-dosage vermicompost treatment. Basidiomycota experienced significant reductions of 34% and 40% in the vermicompost and high-dosage vermicompost treatments, respectively, when compared to CK.

4. Discussion

4.1. Effect of Vermicompost on the Quality of Atractylodes macrocephala

Consistent with numerous research findings, our study confirmed that replacing chemical fertilizers with vermicompost prepared from edible mushroom bran is an organic agricultural management approach. Vermicompost revealed a significant increase in both the yield and levels of the Atractylodes ketone, Atractylodes endocannabinoid II, and β-eudesmol. Vermicompost contains organic matter, nitrogen, phosphorus, potassium, humic acid, amino acids, numerous diverse microorganisms, and other beneficial substances. All available nutrients were essential for plant growth and development, ultimately resulting in improved crop yields, such as chicory [13], saffron [14], garlic [46], and so on. Vermicompost delivered essential nutrients for crop growth and significantly enhanced crop quality, such as garlic [15]. Humic acids present in vermicompost facilitate the synthesis of phenolic compounds, including plant anthocyanins and flavonoids. These compounds contribute to enhanced plant quality and act as natural deterrents against pests and diseases [47,48]. Our result proved that the application of vermicompost improved the quality of Chinese medicine, which has profound significance for enhancing the resource utilization of organic waste and human health [20,21]. Vermicompost application stimulates root system growth, thereby enhancing soil structure, increasing soil fertility, and elevating the soil’s water-holding capacity. It also contributes to improved aeration and drainage by enhancing air and water availability. Simultaneously, vermicompost application enriches the soil with nutrients, increases soil enzyme activity, and enhances productivity.

4.2. Effect of Vermicompost on Soil Nutrient Concentration

Soil organic matter (SOM) stands out as a crucial indicator of soil nutrition. Our prior investigation demonstrated that the utilization of vermicompost amendments significantly enhance SOM content [49]. However, the present study did not increase SOM, total nitrogen, total phosphorus, or total potassium concentrations. This phenomenon is likely attributed to the capacity of Atractylodes macrocephala to assimilate phosphorus from the soil to support its own developmental processes. Phosphorus, as a critical limiting factor for crop growth, has consistently demonstrated its importance in soil ecosystems. In comparison to the control group, the application of two dosages of vermicompost led to a significant increase in the soil available phosphorus (AP) content, suggesting an improved nutritional status. The variations in soil AP could be linked to the improved crop productivity and heightened nutrient uptake. Therefore, the utilization of vermicompost organic fertilizer represents a viable approach that can be implemented in agricultural practices. Given the reduced environmental pollution associated with the production of earthworm compost, it emerges as a more favorable option. The application of VcF and VcF2 significantly reduced α-Glucosidase, leading to a harmonized rate of carbon compound conversion and decomposition, along with nitrogen. This consequently stabilized the retained nitrate nitrogen in the soil, ensuring a stable nitrogen supply to the plant and ultimately leading to higher yields compared to the control group [50].

4.3. Effect of Vermicompost on Soil Microbial Activity, and Community Structure in the Root System of Rhizoma Atractylodis

Extracellular enzymes play a crucial role in soil nutrient cycling and are frequently regarded as important indicators of soil health [51]. The assessment of enzyme activities is essential when utilizing varying dosages of vermicompost organic fertilizer [52,53]. The utilization of vermicompost did not notably enhance the functionality activity of metabolic soil enzymes associated with carbon, nitrogen, and phosphorus transformation, except for the soil α-Glucosidase activity. Through the Pearson correlation between soil enzyme activity and soil physicochemical properties, soil acid phosphatase activity was found to have a negative correlation with the total phosphorus and available phosphorus concentrations. A notable positive correlation was observed between the total carbon (TC) and total nitrogen (TN) levels withβ-Glucosidase (BG) activity, as well as N-acetyl-β-D-gluco- saminidase (NAG). Possibly, the significant influence of rainwater leaching, the specific properties of the local sandy soil, and the reduced effect of fertilization on the soil biochemical processes from spring to autumn could be contributing factors [54,55].
Vermicompost inherently harbors specific endemic microorganisms that integrate into the soil, consequently contributing to the overall number of OTUs in the soil. An increase in the number of fungal operational taxonomic units (OTUs) was observed following the application of vermicompost. Vermicompost enhanced the soil microenvironment and increased the soil nutrient levels, leading to alterations in the interactions among native microorganisms. This, consequently, effectively alleviated the decrease in the microbial population over time. The VcF treatment exhibited a higher count of unique OTUs compared to VcF2.
The addition of vermicompost did not change the soil bacterial diversity. The soil fungal diversity significantly increased in VcF compared to CK. The VcF2 treatment significantly increased both the abundance and diversity of the soil fungi. It is probable that, during the application of organic fertilizer, the fungi present in the vermicompost are introduced into the soil, facilitating colonization [56]. An increased fungal community diversity enhances the breakdown of organic matter, leading to more small-molecule organic carbon in the soil, promoting the growth of Rhizoma Atractylodis.
The soil bacterial diversity indexes such as Chao 1, Shannon, and Simpson remained unchanged with the addition of vermicompost, whereas the soil fungal diversity exhibited a significant increase in VcF compared to CK. The VcF2 treatment significantly increased both the abundance and diversity of the soil fungi. The increased diversity of fungal communities facilitated the ability of fungi to utilize macromolecular organic matter, which, in turn, increased the available small-molecule organic carbon in the soil and promoted the growth of Rhizoma Atractylodis [57].
Vermicompost significantly increased the abundance of Actinobacteriota and WPS-2 bacteria phyla, as well as the Ascomycota fungi phylum. Actinobateria primarily contribute to the decomposition of detritus and the heterotrophic nutrient cycle. Actinobacteria, as plant growth-promoting rhizobacteria (PGPR), possess multifunctional traits that promote plant growth and other beneficial properties [58]. Verrucomicrobiota are recognized for encoding a variety of enzymes that degrade carbohydrates, peptidases, and sulfatases, which makes them well-suited for lignocellulose degradation [59]. The application of vermicompost increased the soil nutrient availability, enhancing the growth of co-trophic groups like Actinobacteria and Proteobacteria. Vermicompost application reduced verrucomicrobiota, as well as the abundance of two basidiomycota.
The application of vermicompost increased the abundance of beneficial bacteria like Burkholderia-Caballeronia-Paraburkholderia and Rhizobium spp. Burkholderia-Caballeronia-Paraburkholderia is a versatile genus capable of degrading various aromatic compounds and facilitating the conversion of nitrogen, phosphorus, and potassium. Burkholderia Caballeronia Paraburkholderia comprises numerous beneficial environmental bacterial species, many of which have positive effects on plants, such as promoting plant growth. Burkholderia converts atmospheric nitrogen into ammonia, enhancing nitrogen cycling in agricultural ecosystems, which boosts nitrogen input and improves plant nitrogen absorption and utilization. Burkholderia bacteria secrete organic acids or acid phosphatase, converting insoluble phosphorus in the soil into a soluble form that plants can directly absorb and utilize, thereby enhancing the plant utilization of soil phosphorus [60]. The short-rooted rhizobia genus can establish a nitrogen-fixing symbiotic relationship with soybeans, reducing the need for nitrogen fertilizer input by fixing atmospheric nitrogen [61]. The application of vermicompost significantly increased the relative abundances of the genera Humicola, Inocybe, Podospora, Pseudaleuria, and Alpinaria. The genera of Humicola, Inocybe, and Podospora belong to the Ascomycota phylum. Humicola produces a variety of enzymes, including cellulases, hemicellulases, ligninases, amylases, glucose isomerases, and other metabolic enzymes. These enzymes are vital for transforming organic waste during fermentation. Podospora is common in fertile soil and aids in breaking down tough lignocellulose as soil nutrients increase. Pseudaleuria has a high metabolic capacity and multifunctional physiological characteristics that are often utilized for the biodegradation of aromatic compounds.
The microbial community structure in the soil was compared using a principal coordinate analysis with the Bray–Curtis algorithm (Figure 7). For the soil bacteria, PC1 and PC2 collectively explained 38.56% and 15.19% of the total variance in the variables, respectively. The vermicompost treatments and the control treatment were clearly separated along the primary axis. The results indicated a significant influence of vermicompost application on the community structure of the soil bacteria. Conversely, no significant variance was found in the bacterial community composition between the two levels of vermicompost. The study showed that using vermicompost significantly affected the fungal composition of the soil. The first principal component (PC1) explained 36.8% of the total variance, while the second principal component (PC2) accounted for 22.65% of the variance. These two elements together represented 59.45% of the total variance.
There was a significant negative correlation between α-Glucosidase and WPS-2, while soil β-Glucosidase showed a positive correlation with Verrucomicrobiota and a significant negative correlation with Patescibacteria. Soil N-Acetylamino Glucosidase activity showed a significant positive correlation with Acidobacteriota, Verrucomicrobiota, and Actinobacteriota. Phenol oxidase showed a significant negative correlation with Patescibacteria and Bacteroidota, while peroxidase was significantly associated with Patescibacteria (Figure 8). These findings emphasize the intricate link between soil enzymes and microbial communities, highlighting their influence on the nitrogen cycle and metabolic processes.

5. Conclusions

The application of vermicompost bio-organic fertilizer significantly increased the yield and quality of Chinese herbal medicine Rhizoma Atractylodis, positively affecting soil health. Vermicompost significantly increased the soil phosphorus content and soil enzyme activity. The vermicompost application did not change the soil bacterial diversity, while it significantly increased the soil fungal diversity. VcF increased the abundance of bacterial phyla such as Actinobacteriota and WPS-2, as well as the fungal phylum Ascomycota. Vermicompost application altered the soil bacteria community structure, but had a stable effect on the soil fungi. Increasing the number of beneficial microbes may be a mechanism through which vermicompost organic fertilizer enhances the yield and quality of Rhizoma Atractylodis.

Author Contributions

B.S. and S.W.: data curation, formal analysis, visualization, and writing—original draft. Y.Z. (Ying Zhang), B.C., P.L., X.Z., Y.W. and M.Z.: investigation and methodology. Y.Z. (Yulan Zhang) and H.X.: funding acquisition, conceptualization, resources, supervision, project administration, and review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Key Research and Development Program of China (grant number 2023YFD1500302), the Strategic Priority Research Program of the Chinese Academy of Sciences (grant number XDA28090100), the Major Program of the Institute of Applied Ecology, Chinese Academy of Sciences (grant number IAEMP202201), and the Liaoning Provincial Department of Science and Technology Project “Liaoning Rural Science-Technology Specialized Action Plan” (grant number 2023JH5/10400146 and 2023JH5/10400149) Liaoning Province Applied Basic Research Program Project (2023JH2/101300070).

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Acknowledgments

The authors thank the reviewers and editor for their insightful comments and constructive suggestions.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Effect of vermicompost on the yield and quality of Rhizoma atractylodis. Note: CK: chemical fertilization and VcF: low-dosage vermicompost. The serial numbers in subfigure (A–E) are labeled. “a” and “b” are used to show the level of statistical significance between various groups.
Figure 1. Effect of vermicompost on the yield and quality of Rhizoma atractylodis. Note: CK: chemical fertilization and VcF: low-dosage vermicompost. The serial numbers in subfigure (A–E) are labeled. “a” and “b” are used to show the level of statistical significance between various groups.
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Figure 2. The effect of vermicompost on soil physicochemical properties. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost BD: Bulk Density, TC: total carbon, TN: total nitrogen, TP: total phosphorus, TK: total potassium, NO3−: nitrate nitrogen, NH4+: Ammonium nitrogen, and AP: available phosphorus. The serial numbers in subfigure (A–H) are labeled. “a” and “b” are used to show the level of statistical significance between various groups.
Figure 2. The effect of vermicompost on soil physicochemical properties. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost BD: Bulk Density, TC: total carbon, TN: total nitrogen, TP: total phosphorus, TK: total potassium, NO3−: nitrate nitrogen, NH4+: Ammonium nitrogen, and AP: available phosphorus. The serial numbers in subfigure (A–H) are labeled. “a” and “b” are used to show the level of statistical significance between various groups.
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Figure 3. The effect of vermicompost on soil physicochemical properties. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. AG, α-Glucosidase; BG, β-Glucosidase; AGal, α-Galactosidase; BGal, β-Galactosidase; NAG: N-acetyl-β-D−glucosaminidase; XYL, Xylanase; PPO, phenol oxidase; and POD, peroxidase. The serial numbers in subfigure (A–H) are labeled. “a” and “b” are used to show the level of statistical significance between various groups.
Figure 3. The effect of vermicompost on soil physicochemical properties. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. AG, α-Glucosidase; BG, β-Glucosidase; AGal, α-Galactosidase; BGal, β-Galactosidase; NAG: N-acetyl-β-D−glucosaminidase; XYL, Xylanase; PPO, phenol oxidase; and POD, peroxidase. The serial numbers in subfigure (A–H) are labeled. “a” and “b” are used to show the level of statistical significance between various groups.
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Figure 4. Effect of vermicompost on gene copy numbers, diversity, and composition of soil bacteria and fungi. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. “a” and “b” are used to show the level of statistical significance between various groups. The serial numbers in subfigure (A–J) are labeled.
Figure 4. Effect of vermicompost on gene copy numbers, diversity, and composition of soil bacteria and fungi. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. “a” and “b” are used to show the level of statistical significance between various groups. The serial numbers in subfigure (A–J) are labeled.
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Figure 5. Effect of vermicompost on the level of bacterial phylum and genus level of soil bacteria. Note: The serial numbers in subfigure (A–D) are labeled. CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost.
Figure 5. Effect of vermicompost on the level of bacterial phylum and genus level of soil bacteria. Note: The serial numbers in subfigure (A–D) are labeled. CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost.
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Figure 6. Effect of vermicompost on the level of phylum of soil bacteria and fungi. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. “a” and “b” are used to show the level of statistical significance between various groups. The serial numbers in subfigure (A–E) are labeled.
Figure 6. Effect of vermicompost on the level of phylum of soil bacteria and fungi. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. “a” and “b” are used to show the level of statistical significance between various groups. The serial numbers in subfigure (A–E) are labeled.
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Figure 7. Analysis of the principal coordinates of soil bacterial and fungi community. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. The serial numbers in subfigure (A,B) are labeled.
Figure 7. Analysis of the principal coordinates of soil bacterial and fungi community. Note: CK: chemical fertilization, VcF: low-dosage vermicompost, VcF2: high-dosage vermicompost. The serial numbers in subfigure (A,B) are labeled.
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Figure 8. Relationships of soil enzymes and microbial taxa. Note: AG, α—Glucosidase; BG, β—Glucosidase; AGal, α—Galactosidase; BGal, β—Galactosidase; NAG: N-acetyl-β-D-glucosaminidase; XYL, Xylanase; PPO, phenol oxidase; and POD, peroxidase.
Figure 8. Relationships of soil enzymes and microbial taxa. Note: AG, α—Glucosidase; BG, β—Glucosidase; AGal, α—Galactosidase; BGal, β—Galactosidase; NAG: N-acetyl-β-D-glucosaminidase; XYL, Xylanase; PPO, phenol oxidase; and POD, peroxidase.
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Sun, B.; Wang, S.; Zhang, Y.; Chen, B.; Li, P.; Zhang, X.; Wang, Y.; Zhao, M.; Zhang, Y.; Xie, H. Enhancement of Rhizoma Atractylodis Quality, Soil Nutrients, and Microbial Characters of Vermicompost Preparations from Spent Mushroom and Cow Dung. Agronomy 2024, 14, 1384. https://doi.org/10.3390/agronomy14071384

AMA Style

Sun B, Wang S, Zhang Y, Chen B, Li P, Zhang X, Wang Y, Zhao M, Zhang Y, Xie H. Enhancement of Rhizoma Atractylodis Quality, Soil Nutrients, and Microbial Characters of Vermicompost Preparations from Spent Mushroom and Cow Dung. Agronomy. 2024; 14(7):1384. https://doi.org/10.3390/agronomy14071384

Chicago/Turabian Style

Sun, Baoyi, Shuqiang Wang, Ying Zhang, Bin Chen, Pengcheng Li, Xianying Zhang, Yonghuan Wang, Mingyi Zhao, Yulan Zhang, and Hongtu Xie. 2024. "Enhancement of Rhizoma Atractylodis Quality, Soil Nutrients, and Microbial Characters of Vermicompost Preparations from Spent Mushroom and Cow Dung" Agronomy 14, no. 7: 1384. https://doi.org/10.3390/agronomy14071384

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