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Article

The Combination of Biochar and Phosphorus-Containing Materials Can Effectively Enhance the Remediation Capacity of Amaranth on Cadmium-Contaminated Soil and Improve the Structure of Microbial Communities

by
Zhiyang Jiang
1,
Hongmei Hua
1,
Zheng Yin
2,
Tingsen Wu
3,
Yuzhi Zhou
1,4,*,
Daokun Chen
5,
Xinbin Li
5,
Mingze Zhao
1 and
Wenshuo Wang
1
1
School of Earth and Environment, Anhui University of Science and Technology, Huainan 232001, China
2
School of Chemistry and Chemical Engineering, South China University of Technology, Guangzhou 510641, China
3
School of Earth Resources and Materials Engineering, RWTH Aachen University, 52062 Aachen, Germany
4
Anhui Province Engineering Laboratory of Water and Soil Resources Comprehensive Utilization and Ecological Protection in High Groundwater Mining Area, Huainan 232001, China
5
Xi’an Center of Mineral Resources Survey, China Geological Survery, Xi’an 710119, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(10), 2300; https://doi.org/10.3390/agronomy14102300 (registering DOI)
Submission received: 10 July 2024 / Revised: 25 September 2024 / Accepted: 1 October 2024 / Published: 6 October 2024
(This article belongs to the Section Soil and Plant Nutrition)
Browse Figures
Versions Notes

Abstract

:
Cadmium (Cd) pollution in soil has become a huge problem for agricultural production in China and even the world. Passivation and phytoremediation are two important remediation technologies for Cd pollution. In this study, the cadmium-contaminated and phosphorus-poor farmland soil around a mining area in Huainan was taken as the research object, and the remediation effect of biochar and phosphorus-containing materials on soil cadmium pollution was discussed. The results showed that the combined application of biochar and phosphorus-containing materials significantly reduced the pH of non-rhizosphere soil and rhizosphere soil, and increased the content of soil dissolved organic carbon (DOC). The combined application of biochar and phosphorus-containing materials significantly reduced soil pore water Cd and soil available Cd. In addition, both a single application of biochar and synergistic application of biochar and phosphorus-containing materials significantly increased the biomass of aboveground and underground parts of amaranth and soil urease and catalase activities. Phosphorus application reduced the bioavailability of Cd in soil. With the increase in phosphorus application, the content of available Cd in soil decreased significantly, and there was a certain negative correlation between Cd content and phosphorus content in plants. The abundance of beneficial microorganisms such as Ochrobactrum, Anaerolinea, Achromobacter, and Cellvibrio in soil was significantly increased after the synergistic application of biochar and phosphorus-containing materials.

1. Introduction

Healthy soil is the basis for human survival and development. In recent years, due to the rapid development of China‘s modernization and industrialization, soil heavy metal pollution has become increasingly serious. Cd, as a carcinogenic heavy metal [1], easily enters the human body through the food chain after being accumulated by plants, and then causes serious damage to human organs [2]. At the same time, the source of Cd pollution in soil is mainly discharged into farmland by atmospheric deposition, wastewater irrigation, and fertilization [3]. According to statistics, Cd is the element with the highest over-standard rate among heavy metal pollution elements in China, and the over-standard points account for 7% [4]. Huainan City in the study area is an important industrial and coal city in eastern China. Long-term coal mining and large-scale industrial production have caused serious soil heavy metal cadmium pollution in this area. Lime concretion black soil is the most common soil type in the inter-river plain of Huainan City. Cd pollution not only restricts the development of local agriculture, but also causes harm to the health of local residents [5]. In addition, due to the differences in soil parent materials, phosphorus deficiency is common in lime concretion black soil, which seriously affects the growth of soybeans, wheat, and other crops [6]. Therefore, it is imperative to find a feasible technology to repair cadmium-contaminated soil while providing phosphorus to meet plant growth.
Due to the high cost and long treatment period of soil cadmium pollution, it is particularly important to explore an economical, efficient, green, and feasible remediation technology. At present, among many soil remediation technologies, in situ immobilization with passivators is regarded as a simple and efficient Cd-contaminated farmland soil remediation strategy [7]. Common passivators such as zeolite, sepiolite, attapulgite, etc., which have high cation exchange capacity, can reduce the availability of cadmium in soil through adsorption, ion exchange, complexation, and precipitation [8,9]. Amirahmadi et al. [10] studied the effects of adding different doses of natural zeolite to cadmium-contaminated soil on maize growth, soil aggregate stability, and nutrient availability. It was found that an appropriate amount of zeolite can not only significantly improve maize growth and soil quality, but also reduce the bioavailability of cadmium. However, excessive doses may destroy soil structure. Zhao et al. [11] showed that zeolite could significantly reduce the content of available Cd in soil and inhibit the absorption of Cd by rice. Biochar is famous for its low cost and environmental friendliness, which is due to its rich pore structure, large specific surface area, and many oxygen-containing functional groups. It can effectively reduce the mobility and bioavailability of heavy metals, and has been widely used in the remediation of heavy metal-contaminated soil [12,13]. For example, Shi et al. [14] used the adsorption, precipitation, and chelation of biochar to reduce the biological toxicity of Cd in soil. Xia et al. [15] found that after biochar was applied to the soil, the bioavailability, toxicity, and accumulation of heavy metals such as cadmium and lead in plants showed different degrees of decline. It has also been found that biochar can change soil physical and chemical properties and microbial community structure, thus affecting the availability of heavy metals in soil [16,17]. In addition, phytoremediation has gradually attracted people‘s attention because of its simple operability and low cost and no re-pollution. It is an environmentally friendly remediation method with wide application potential [18]. Planting hyperaccumulators in cadmium-contaminated soil can significantly enhance the remediation effect of contaminated soil and reduce the concentration of heavy metal cadmium in the soil to a tolerable range [19]. Therefore, exploring how plants absorb and transport Cd, and their tolerance mechanisms, is of great importance to solve the problem of Cd-contaminated soil [20]. For example, Chi et al. [21] found that changes in root exudates affect the bacterial community and thus reduce the availability of cadmium through hyperaccumulative plant-crop intercropping. Feng et al. [22] found that the absorption of Cd in rice plants was significantly related to the availability of cadmium in soil through long-term experiments. In order to enhance the remediation effect of hyperaccumulators on contaminated soil, fertilization is regarded as a key auxiliary means. It not only provides necessary nutrition for plant growth, but also may affect the activity of heavy metals in soil [23,24]. However, lime concretion black soil, as a representative of typical soil in Huainan City, has not only been affected by Cd pollution caused by local coal mining for a long time, but its own phosphorus content is also poor, which leads to poor plant growth. If fertilization and other methods are used to enhance the absorption and enrichment ability of existing plants to cadmium, it will be a win–win strategy. In other words, while repairing soil cadmium pollution in the region, it will be a win–win strategy. It also takes into account the improvement in soil fertility.
In recent years, the research on biochar and phosphate fertilizer in improving crop yield has gradually increased, but the application in the field of phytoremediation is relatively small; especially when the two fertilizers are used in combination, the effect is not yet clear. In this paper, a pot experiment was conducted to study the effects of different levels of phosphorus-containing materials on the growth of Amaranshus mangostanus L. and the absorption and accumulation of Cd and P. The effects of biochar and phosphorus-containing materials on soil health were evaluated by soil enzyme activity and microbial community structure through high-throughput sequencing technology. The aim is to provide a green and sustainable remediation method for heavy metal pollution in farmland soil, and provide the necessary technical support for large-scale, high-intensity safe use.

2. Materials and Methods

2.1. Experimental Materials

The tested phosphate fertilizer was ammonium dihydrogen phosphate (NH4H2PO4, analytically pure). The test crop was Cd hyperaccumulator amaranth, and the variety was Amaranshus mangostanus L.

2.1.1. Tested Biochar Materials

The preparation of biochar was obtained from the abandoned soybean straw in the above farmland, which was dried and crushed naturally, and then carbonized by a 2 mm nylon sieve through a muffle furnace at 400 °C under anaerobic conditions. The pH value was 9.25, the organic matter content was 396.62 g·kg−1, the total nitrogen content was 7.66 g·kg−1, the total phosphorus content was 0.76 g·kg−1, the total potassium content was 0.68 g·kg−1, and the Cd content was 0.02 mg·kg−1.

2.1.2. Soil Sampling and Analysis

The test soil samples were collected from the farmland soil in Beiliwan, Xiataocun Village, Shungeng Town, along the south bank of Huaihe River. The surface soil samples of 0–20 cm were dug, and 5 samples were collected by the double-diagonal method. After uniform mixing, 500 g samples were retained by the quartering method for soil index determination, and naturally air-dried, and foreign bodies such as stone particles and plant roots contained in the soil were removed, ground through a 2 mm nylon sieve, and bagged for later use. The basic physical and chemical properties of soil: pH = 7.95, organic matter content (w) was 11.04 g·kg−1, total nitrogen content was 0.57 g·kg−1, available phosphorus content was 34.36 mg·kg−1, available potassium content was 85.02 mg·kg−1, and total soil cadmium content was 0.95 mg·kg−1.

2.1.3. Pot Experiment

The indoor amaranth pot experiment was carried out. The collected soil samples were air-dried and ground through a 4 mm sieve for later use. Biochar and phosphorus-containing materials (potassium dihydrogen phosphate, analytically pure) were used as repair materials and applied to the soil according to different concentration gradients. The specific treatment was set as follows: a blank control (CK), single application of 2.5% biochar (T1), 2.5% biochar combined with 0.5 g phosphorus-containing material (T2), 2.5% biochar combined with 1 g phosphorus-containing material (T3), 2.5% biochar combined with 2 g phosphorus-containing material (T4). Each treatment was set up with 4 replicates and 1 kg soil per pot. In addition, nitrogen and potassium were supplemented with urea and potassium sulfate, and the addition amount of each pot was N 500 mg·kg−1 soil and K 500 mg·kg−1 soil.
The air-dried and ground soil, biochar, and phosphorus-containing materials were evenly mixed and loaded into plastic pots. We added water to each pot to 60% of the field capacity. After one month, amaranth was sown. After one week of emergence, the seedlings were planted, with 5 plants in each pot, and deionized water was regularly poured during the growth period. After 10 days of amaranth planting, the pore water collector was inserted into the amaranth pot near the root part of amaranth, and the soil pore water was collected every 7 days to determine the cadmium content in the soil pore water. After the amaranth matured, amaranth plant samples, root soil samples, and non-root soil samples were collected.
The amaranth was harvested after 45 days of growth. The sludge and impurities on the plant samples were fully washed with pure water on the shoots and roots, respectively. The green was killed at 105 °C for 30 min, and the oven was dried at 60 °C to a constant, and the dry weight was measured. Finally, it was crushed and passed through a 100-mesh sieve for use.
At the time of amaranth harvest, 4–5 cm soil near the root system was collected, and part of it was put into a sterilized 20 mL centrifuge tube and stored in a refrigerator at −80 °C for the determination of soil microbial indicators. Some samples were stored in a refrigerator at 4 °C for the determination of soil enzyme activity. The remaining soil samples were taken to 500 g by the quartering method, which were used to determine soil chemical properties and heavy metals, respectively.
Superaccumulative amaranth follow-up treatment: For the hyperaccumulative plants that adsorb heavy metals, our treatment method was to store them in the local industrial waste residue or coal gangue dump, and then burn them to prevent the heavy metals adsorbed by the plants from entering the soil again after the death of the plants.

2.1.4. Index Test Method

Soil chemical properties referred to the method of Bao et al. [25] as follows: Soil pH was measured with a pH meter according to the soil–water ratio of 1:2.5. Soil electrical conductivity (EC) was measured by an electrical conductivity meter according to the soil–water ratio of 1:5. Soil organic matter (OM) content was determined by the potassium dichromate volumetric method. Soil DOC was extracted at a water–soil ratio of 1:5 and determined using a TOC analyzer (TOC-L CPN, Shimadzu, Kyoto, Japan). Soil available phosphorus was determined by the 0.5 mol/L NaHCO3 extraction–molybdenum antimony colorimetric method.
Soil enzyme activity referenced the Guan et al. [26] method, the determination of soil H2O2 enzyme activity using KMnO4 titration, and urease activity using the indophenol blue colorimetric method.
The soil available Cd content was extracted with 0.01 mol/L CaCl2 at a soil–water ratio of 1:5, and the soil samples were digested with hydrochloric acid–nitric acid–hydrofluoric acid. The Cd content in the digestion solution was determined by atomic absorption spectrophotometry (PE-PinAAcle 900 T, PerkinElmer, Waltham, MA, USA). In the process of the sample analysis, Chinese national standard material soil (GBW07430, Chinese Academy of Geological Sciences, Langfang, China) was added for quality control; a blank test and standard addition recovery were carried out in the whole process, and the standard addition recovery rate of the heavy metal detection process was controlled at Cd 90–110%. The plant samples were digested by HNO3–HClO4, and the Cd content was determined by ICP-AES [27].
Soil microbial determination was based on 16S rRNA high-throughput sequencing technology; a small fragment library was constructed for sequencing by using the double-end sequencing method. Through the read splicing filtering, OTU clustering, species annotation, and abundance analysis, the sample species composition was revealed.

2.1.5. Data Processing and Analysis

The preliminary analysis of the test data was carried out by Microsoft Excel 2016. The test data were expressed by three replicates (mean ± standard deviation). SPSS 23 was used for a statistical analysis of the data. Canoco5 Tutorial, Origin 2021 b, and Microsoft Excel 2016 were used for mapping.
Combined with plant biomass, the ability to absorb and accumulate heavy metal Cd was reflected by calculating the plant bioconcentration factor and translocation factor. The calculation formulae [28] are as follows:
  • Bioconcentration factor (BCF) = Cd content in shoots/Cd content in soil;
  • Transfer coefficient (TF) = shoot Cd content/root Cd content;
  • Cadmium accumulation in aboveground part of plant = Cd content in aboveground part of plant × aboveground biomass of plant;
  • Cadmium accumulation in plant roots = Cd content in plant roots × biomass in plant roots.

3. Results and Analysis

3.1. Effects of Different Treatments on Soil Properties and Available Cadmium

3.1.1. Effects of Different Treatments on Soil pH and DOC

It can be seen from Figure 1 that the application of biochar alone (T1) significantly increased the pH value of the soil (p < 0.05), in which the pH value of the non-rhizosphere soil increased by 0.84 units, while the pH value of the rhizosphere soil increased by 0.28 units. Compared with the single application of biochar (T1), the mixed application of phosphorus-containing materials and biochar (T2, T3, T4) resulted in a decrease in soil pH. The specific performance was that the pH value of non-rhizosphere soil decreased by 0.43 to 1.24 units, and the pH value of rhizosphere soil decreased by 0.13 to 0.68 units. With the increase in the amount of phosphorus-containing materials, the pH values of non-rhizosphere soil and rhizosphere soil showed a significant decrease (p < 0.05). Compared with CK, T1 and T2 treatments significantly reduced soil pH (p < 0.05), while T3 and T4 had no significant effect on the non-rhizosphere soil and rhizosphere (p < 0.05). From the overall trend of the soil pH value, in the mature period of amaranth, the pH value of non-rhizosphere soil is generally higher than that of rhizosphere soil.
It can be found from Figure 2 that the content of dissolved organic carbon (DOC) in the non-rhizosphere area of the soil was lower than that in the rhizosphere area at the maturity stage of amaranth. Compared with CK, the combined application of biochar and phosphorus-containing materials (T1, T2, T3) significantly increased the DOC content in rhizosphere soil and non-rhizosphere soil. Compared with the single application of biochar (T1), the mixed application of phosphorus-containing materials and biochar significantly reduced the DOC content in the rhizosphere soil (p < 0.05). Under the treatment conditions of T2, T3, and T4, the DOC content decreased by 5.6%, 3.9%, and 9.3%, respectively. In general, T1, T2, and T3 treatments significantly increased the DOC content in non-rhizosphere and rhizosphere soils (p < 0.05), while T4 treatment had no significant effect on the DOC content in non-rhizosphere and rhizosphere soils (p < 0.05).

3.1.2. Effects of Different Treatments on Cadmium Concentration in Soil Pore Water

During the whole growth period of amaranth, the Cd concentration in soil pore water under different treatments increased first and then decreased. In general, the Cd concentration in soil pore water under each repair material treatment was in a low range (Figure 3). The changes in Cd concentration in soil pore water of all treatment groups were similar. During the first 0 to 14 days, the Cd concentration in soil pore water gradually increased until it reached the peak on the 14th day, and then decreased rapidly, reaching the lowest point on the 42nd day. Compared with the CK treatment group, T1, T2, T3, and T4 treatments all reduced the Cd concentration in soil pore water. After 42 days of amaranth ripening, the Cd concentration in soil pore water was CK > T4 > T3 > T2 > T1. The peak value of Cd in soil pore water of each treatment group corresponds to about 14 days. This stage may be the development period of amaranth growth. Its roots had a strong absorption effect on water and soil nutrients. The high nutrients contained in soil pore water would force Cd to leach from the soil surface, so this peak will appear.

3.1.3. Effects of Different Treatments on Soil Available Cadmium Content

The content of available cadmium in soil is shown in Figure 4. It can be seen that compared with CK treatment, T1, T2, T3, and T4 treatments significantly reduced the content of available cadmium in soil (p < 0.05), T3 (10.58%) > T2 (8.23%) > T1 (4.71%). Compared with T1 treatment, T2, T3, and T4 treatments significantly reduced the content of available Cd in soil (p < 0.05), indicating that the availability of Cd in soil decreased with the increase in phosphorus-containing materials.

3.1.4. Effects of Different Treatments on Soil Enzyme Activity

The results of soil catalase and urease activity are shown in Figure 5. It can be seen that T1, T2, T3, and T4 treatments significantly increased the activity of catalase and urease in soil (p < 0.05). Among them, T1 treatment was 2.81 times and 2.42 times higher than CK, T2 treatment was 2.66 times and 2.25 times higher than CK, T3 treatment was 2.34 times and 2.12 times higher than CK, and T4 treatment was 2.31 times and 2.06 times higher than CK.

3.2. Effects of Different Treatments on Growth and Cadmium Accumulation of Amaranth

3.2.1. Effects of Different Treatments on Biomass of Amaranth in Cadmium-Contaminated Soil

In the lime concretion black soil with a cadmium pollution concentration of 0.95 mg·kg−1 soil, compared with the CK treatment group, the aboveground and root biomass of amaranth increased significantly in different treatment groups. The order of biomass increase in each treatment group was as follows: T4 > T3 > T2 > T1 (Figure 6). A further analysis showed that the aboveground biomass of amaranth increased by 58.15–164.13%, and the root biomass increased by 50.19–171.85%, and there were significant differences among the treatment groups. The above results showed that a single application of biochar or biochar combined with phosphorus-containing materials could significantly promote the growth of amaranth, and the increase in plant biomass was the most significant under a high phosphorus application level.

3.2.2. Effects of Different Treatments on Absorption and Accumulation of Cadmium in Amaranth

As shown in Table 1, compared with CK, the Cd content in the shoots and roots of amaranth under different treatments (T1, T2, T3, T4) decreased significantly (p < 0.05), (T4 > T3 > T2 > T1). A further analysis showed that the Cd content in shoots and roots of amaranth decreased by 16.8–47.02% and 23.15–59.16%, respectively. With the increase in the amount of biochar combined with phosphorus-containing materials, the Cd content of amaranth decreased, but the transport coefficient of amaranth increased with the increase in phosphorus application. Therefore, the application of phosphorus-containing materials could promote the absorption and transport of Cd in the aboveground part of amaranth, indicating that Cd was mainly enriched in the aboveground part and could reduce the Cd content in the soil.
The accumulation of Cd increased under different treatments, and the increase in Cd accumulation in the aboveground part of amaranth under different treatments was T3 > T2 > T4 > T1, with an increase of 30.24–39.14%. The increase in Cd accumulation in amaranth roots under different treatments was T3 > T1 > T4 > T2, with an increase of 9.63−20.59%. A further analysis showed that the Cd accumulation in the shoot and root of amaranth was the highest under T3 treatment, and the values were 3.91 and 7.26 μg pot−1, respectively. In this experiment, the mixed application of biochar and phosphorus-containing materials could effectively increase the accumulation of Cd in amaranth. When the dosage of biochar combined with phosphorus-containing materials was 1 g/pot soil, the accumulation of Cd in plants was the largest, which further improved the remediation efficiency of Cd-contaminated soil.

3.2.3. Effects of Different Treatments on Phosphorus Uptake and Accumulation in Amaranth

It can be seen from Figure 7 and Figure 8 that compared with CK treatment, the phosphorus content in the aboveground part and root of biochar (T1) treatment was 0.85 and 0.71 mg·kg −1, respectively, which was about 2.3% and 4.2% higher than that of the control group CK, and the phosphorus accumulation was 1.85 and 1.35 μg·pot−1, respectively, which was about 37.83% and 36.29% higher than that of the control group CK, respectively. Compared with CK treatment, biochar combined with different amounts of phosphorus-containing materials (T2, T3, T4) significantly increased the phosphorus content and accumulation in the shoots and roots of amaranth (p < 0.05).
Different fertilization schemes had a significant effect on the phosphorus content and total phosphorus accumulation of amaranth plants. There were significant differences between these treatments; especially when the P level reached 2 g/pot soil, the effect was the most significant, which was significantly higher than other treatment methods (p < 0.05). With the increase in the application amount of phosphorus-containing materials, the phosphorus content and its accumulation in amaranth plants also showed an upward trend. This indicated that the absorption and accumulation of phosphorus in amaranth were restricted by the level of phosphorus application, and increased with the increase in phosphorus application.

3.3. Effects of Different Treatments on Soil Microbial Diversity and Community Structure

3.3.1. Microbial Community Structure in Rhizosphere Soil

The community structure of dominant bacteria in rhizosphere soil at the phylum level and genus level are shown in Figure 9 and Figure 10, respectively. It can be seen from Figure 9 that the relative abundance of soil microorganisms at the phylum level could be classified into seven dominant species. They were Chloroflexi (28.53–40.46%), Proteobacteria (20.92–31.75%), Actinobacteria (8.03–11.56%), Gemmatimonadetes (7.16–7.64%), Cyanobacteria (4.39–6.82%), Acidobacteria (5.31–8.55%), and Bacteroidetes (3.82–8.13%). Compared with CK, the relative abundance of Proteobacteria under T1, T2, T3, and T4 treatments increased significantly after the application of biochar and phosphorus-containing materials, while the relative abundance of Chloroflexi decreased significantly. More precisely, compared with CK, the relative abundance of Chloroflexi, Actinobacteria, and Acidobacteria decreased by 14.3, 23.44, and 18.12 percentage points, respectively, while the relative abundance of Proteobacteria, Cyanobacteria, and Gemmatimonadetes increased by 19.98, 21.86, and 6.13 percentage points, respectively. Compared with CK, under the combined application of biochar and phosphorus-containing materials (T2, T3, T4), Proteobacteria, Cyanobacteria, Gemmatimonadetes, Bacteroidetes, and Firmicutes increased by 29.16–51.76, 38.04–55.35, 5.71–7.11, 90.31–108.37, and 16.60–26.71 percentage points, respectively. Chloroflexi, Actinobacteria, and Acidobacteria decreased by 18.85–29.48, 26.64–31.92, and 26.78–37.89 percentage points, respectively. In addition, with the increase in the amount of phosphorus-containing materials, the relative abundance of Chloroflexi, Actinobacteria, and Acidobacteria decreased, while the relative abundance of Proteobacteria, Cyanobacteria, and Bacteroidetes increased.
At the level of soil microbial genera, the microbial community structure of each treatment changed significantly. Among them, Kaistobacter, Lysobacter, Mermoricola, Candidatus Koribacter, and Candidatus Solibacter were the dominant microorganisms with a relatively high abundance in the CK treatment soil. Compared with CK treatment, new dominant genera appeared in T1, T2, T3, and T4 treatment groups, including Cellvibrio, Actinotalea, Ochrobactrum, and Achromobacter. The dominant microbial genera in T1, T2, T3, and T4 treatment soils were similar, including Kaistobacter, Lysobacter, Mermoricola, Anaerolinea, and Ochrobactrum. In addition, the dominant genus of T2 treatment also included Cellvibrio, and the dominant genus of T3 and T4 treatment also included Achromobacter.

3.3.2. Analysis of Relationship

A Pearson correlation analysis was performed on soil properties and microbial communities. The results are shown in Figure 11 and Figure 12. At the level of the microbial phylum, Chloroflexi was significantly positively correlated with Actinobacteria and DTPA-Cd, and Chloroflexi was significantly negatively correlated with Firmicutes, Proteobacteria, and Cyanobacteria. Proteobacteria were significantly positively correlated with Cyanobacteria, Gemmatimonadetes, and Firmicutes, and significantly negatively correlated with Acidobacteria and DTPA-Cd. Actinobacteria were significantly negatively correlated with Gemmatimonadetes and Bacteroidetes. Cyanobacteria were significantly positively correlated with Gemmatimonadetes and Firmicutes, and significantly negatively correlated with DTPA-Cd. Acidobacteria were significantly positively correlated with DTPA-Cd and significantly negatively correlated with Firmicutes. Gemmatimonadetes was significantly positively correlated with Bacteroidetes. Firmicutes was significantly negatively correlated with DTPA-Cd. EC was significantly positively correlated with URE and CAT.
At the genus level (Figure 12), Lysobacter was significantly positively correlated with DTPA-Cd and Rhodoplan, and significantly negatively correlated with Blastococcus, Cellvibrio, Achromobacter, Clostridium, and Mesorhizobium. Blastococcus was significantly positively correlated with Cellvibrio, Clostridium, and Mermoricola, and significantly negatively correlated with DTPA-Cd. Cellvibrio was significantly positively correlated with Achromobacter and Clostridium, and significantly negatively correlated with Rhodoplan and DTPA-Cd. Actinotalea was significantly positively correlated with EC, URE, and CAT. Rhodoplan was significantly negatively correlated with Anaerolinea, Ochrobactrum, and Achromobacter. Both Sphingobium and Mesorhizobium were significantly negatively correlated with DTPA-Cd.
In order to further explore the relationship between soil properties and microbial communities at the phylum level and soil DTPA-Cd, an RDA analysis was performed, and the results are shown in Figure 13. The results showed that the variation interpretation rates of the first axis and the second axis were 93.10% and 6.59%, respectively, and the cumulative interpretation rate was 99.69%. Soil DTPA-Cd concentration was negatively correlated with soil EC, URE, and CAT, and negatively correlated with the relative abundance of Bacteroidetes, Gemmatimonadetes, Cyanobacteria, Proteobacteria, and Firmicutes. In addition, soil DTPA-Cd concentration was positively correlated with the relative abundance of Actinobacteriota, Chloroflexi, and Acidobacteria. There was a negative correlation between the relative abundance of Proteobacteria and Bacteroidota.

4. Discussion

4.1. Causes of Changes in Soil pH and DOC Content

As shown in Figure 1, biochar helped to increase the pH of rhizosphere and non-rhizosphere soils because the tested biochar had a high pH (9.25) and the hydrolysis of alkaline components (such as carbonates and phosphates) in biochar increased the OH− content in the soil [29]. The pH values of rhizosphere and non-rhizosphere soils decreased gradually with the increase in the amount of phosphorus-containing materials. This was due to the fact that potassium dihydrogen phosphate, as an acidic material, could be electrolyzed into the soil to produce H+, resulting in a decrease in pH [30]. Microorganisms in the soil released a large amount of carbon dioxide in the interaction with plant respiration. At the same time, the roots of plants produced acidic secretions to improve the availability of soil nutrients around the rhizosphere, such as acid phosphatase and organic acids (carboxylates) [30,31,32,33], resulting in a higher pH in the non-rhizosphere soil of amaranth than in the rhizosphere soil at maturity. DOC was mainly composed of humus, humic acid, and fulvic acid. These components showed high activity for bound ions, organic molecules, and solid surfaces in soil [34]. Studies have shown that DOC content was largely regulated by pH. For example, Kim et al. [35] found that the increase in soil pH would increase the activity of microorganisms and the solubility of DOC. In this study, after the addition of biochar, the pH value of the soil increased, which might increase the content of DOC, and the active organic carbon components in biochar might be released into the soil, which would also lead to the increase in DOC content in the soil.

4.2. Effects of Different Treatments on the Change in Cadmium Content in Soil Pore Water

During the whole growth period of amaranth, the Cd concentration in soil pore water of different treatments increased first and then decreased. In general, under various treatment conditions, the Cd concentration in soil pore water was lower than the initial level. The increase in Cd concentration in pore water of soil was mainly due to the competition between soluble organic carbon and heavy metals on the adsorption position of the surface of the repair material, which enhanced the migration ability of heavy metals. During the treatment of biochar and phosphorus-containing materials, the DOC content in the soil increased, which led to the activation of some Cd, thereby enhancing its migration ability. The decrease in Cd concentration in soil pore water in the later stage was due to the adsorption and chelation of active functional groups such as carboxyl and hydroxyl groups in the repair material, which made its mobility in the soil and the concentration of soil pore water lower than that of the blank control group [36].

4.3. Effects of Different Treatments on Soil Available Cadmium Content

The part of heavy metals in soil that could be directly absorbed and utilized by plants in their effective state was determined by the degree of risk of heavy metals in soil to the environment.
It is not difficult to see from Figure 4 that the content of available cadmium could be significantly reduced by a single application of biochar or a mixed application of biochar and phosphorus-containing materials. On the one hand, due to the rich functional groups in biochar, the single bond of carbon and hydrogen and the single bond of carbon and oxygen had an adsorption effect on Cd, which will reduce the effectiveness of Cd in soil [37]. On the other hand, the application of alkaline-dependent biochar into the soil increased the soil pH and promoted the formation of metal precipitation Cd(OH)2, which was similar to the conclusion of Sun et al. [38]. In addition, some scholars have also found that biochar added to the soil would gradually age and produce more oxygen-containing functional groups, which was conducive to the fixation of heavy metals in the soil [39].
Compared with the single application of biochar (T1), the mixed application of phosphorus-containing materials and biochar (T2, T3, T4) had a better immobilization effect on Cd. Since the content of TP and AP in the soil mixed with phosphorus-containing materials and biochar was significantly higher than that of a single application of biochar, the increase in AP promoted the formation of Cd3(PO4) 2, Cd5(PO4)3OH, and Cd5(PO4)3Cl [40], which played an important role in reducing the effectiveness of Cd in soil. Huang et al. [41] found that there was a strong negative correlation between soil available phosphorus and available Cd. The increase in soil phosphorus content would promote the complexation reaction between soil phosphorus and Cd in soil, enhance the fixation of Cd, and reduce the content of available Cd in soil. This negative correlation was more obvious with the increase in phosphorus application. In addition, all treatments significantly promoted the increase in dissolved organic carbon (DOC) content in soil, which in turn strengthened the binding between DOC and cadmium in soil. The enhancement in this effect led to the decrease in bioavailability of heavy metal cadmium, which might reduce the potential toxicity and ecological risk of heavy metals to organisms [42].

4.4. Effects of Different Treatments on Soil Enzyme Activity

Soil enzymes were directly involved in soil biochemical processes and were highly sensitive to changes in soil physical and chemical properties and other environmental factors [43]. Their activity could largely characterize the effect of soil remediation [44]. This study found that the single application of biochar or the mixed application of biochar and phosphorus-containing materials significantly increased the activity of urease and catalase in soil. This might be because biochar increased soil pH, reduced the activity of heavy metals, and reduced the toxic effects of heavy metals, resulting in increased enzyme activity [45]. Compared with the single biochar treatment group T1, with the increase in the amount of phosphorus-containing materials (T2, T3, T4), the activities of urease and catalase decreased. This might be because the phosphorus-containing materials caused the soil pH to decrease, which further led to the decrease in enzyme activity, which was consistent with the results of other scholars. For example, the results of Pei et al. [46] also showed that soil enzyme activity was significantly positively correlated with soil pH and negatively correlated with soil available cadmium content. Kotroczó et al. [47] found that with the increase in soil pH, the activities of catalase, polyphenol oxidase, and urease in soil also increased. Feyissa et al. [48] found that soil pH regulates the soil enzyme activity and stoichiometric ratio by affecting microbial biomass distribution and substrate solubility. It could be seen that the activity of heavy metals in soil and the physical and chemical factors such as the pH value and AP were the core elements that determined the activity of soil enzymes.

4.5. Effects of Different Treatments on the Growth of Amaranth in Cadmium-Contaminated Soil

This study shows that T1, T2, T3, and T4 treatments significantly increased the biomass of aboveground and underground parts of amaranth, and the biomass of T4 treatment was significantly higher than that of other treatment groups, indicating that the application of biochar and phosphorus-containing materials could significantly promote the growth of amaranth, and the synergistic effect of the two was the best. Tang et al. [23] also obtained similar results; that is, pot experiments showed that the addition of nitrogen and phosphorus fertilizers in contaminated soil promoted the dry weight, plant height, and root length of soil plant communities, and increased with the increase in phosphorus fertilizer application, which accelerated the absorption of soil heavy metals by plants. Therefore, in the process of the remediation of cadmium-contaminated soil, the appropriate use of phosphate fertilizer could increase the biomass of hyperaccumulators, thereby improving the remediation effect, and the accumulation of Cd was the largest under high phosphorus treatment (T4).

4.6. Effects of Different Treatments on the Absorption and Accumulation of Cadmium and Phosphorus in Amaranth

There was a close relationship between phosphorus and cadmium in soil, and the effectiveness of cadmium in soil would be restricted by phosphorus to a certain extent [49]. This experiment found that the application of biochar and phosphorus-containing materials significantly reduced the content of available Cd in soil, and the content of available Cd in soil decreased the most under high phosphorus treatment (T4). When phosphorus-containing materials were applied to the soil, the chemical reaction was quite complex, and phosphate could affect the effectiveness of cadmium by inducing adsorption and precipitation mechanisms [50]. Studies have shown that phosphorus-containing materials could convert more exchangeable cadmium into more stable residual Cd, and further stabilize soil cadmium [51]. Li et al. [52] found that the abundance of available phosphorus in the soil provided by biochar and phosphate fertilizer created conditions for the occurrence of precipitation, and promoted the transformation of carbonate and organic cadmium forms to the residual cadmium part. The mechanism of cadmium precipitation in the XRD pattern of cadmium-containing minerals further explained that high phosphorus input could improve the fixation efficiency of cadmium. Chen et al. [53] showed that Cd could co-precipitate with FeS or replace Fe in FeS under anoxic conditions. It was also found that with the increase in exogenous phosphate ions, the number of negative charges on the soil surface increased and further aggravated the adsorption capacity of Cd ions, so that heavy metals continued to exist in the form of electrostatic adsorption around soil particles, thereby reducing the effective state of Cd [40,54].
In this experiment, it can be seen from Figure 14 that the content of phosphorus and the content of Cd in amaranth showed a certain degree of negative correlation. With the gradual increase in phosphorus content, the content of Cd began to decrease gradually. The application of phosphate fertilizer could significantly promote the absorption of phosphorus by plant roots and reduce the Cd content of amaranth [55,56]. This was consistent with the results of this study. The application of phosphate fertilizer might lead to the decrease in Cd content in amaranth plants, which might be due to the effect of phosphorus on the activity of heavy metals in soil and the absorption and accumulation of crops [57]. This study showed that with the increase in the phosphorus application rate, the Cd accumulation in the aboveground part and roots of amaranth plants was higher than that of CK, which was consistent with the results of Bauddh et al. [58]. All in all, the combined application of biochar and phosphorus-containing materials could promote the growth and development of amaranth roots, expand the contact area between roots and soil, and increase the opportunity to absorb Cd, thereby increasing the accumulation of Cd in amaranth. Although the Cd content in amaranth decreased with the increase in the application amount of phosphorus-containing materials, the increased biomass greatly increased the total absorption and accumulation of Cd in amaranth, and generally improved its bioremediation efficiency.

4.7. Effects of Different Treatments on Soil Microbial Community Structure

Soil remediation not only takes into account the reduction in soil availability, but also needs to pay attention to changes in soil environmental health. The soil microbial community plays an important role in the migration and transformation of heavy metals, which can be used as an evaluation index of soil health quality [59]. In this study, high-throughput sequencing technology was used to analyze the microbial community structure in each treated soil in detail. The results showed that at the phylum level, the most abundant microbial community composition in the control soil was Chloroflexi, Proteobacteria, and Actinobacteria, which was similar to the results of other heavy metal-contaminated soils [60,61]. Compared with CK, the relative abundance of Chloroflexi and Actinobacteriota in soil decreased significantly after adding biochar, while the relative abundance of Proteobacteria increased significantly. It is well known that Chloroflexi prefers nutrient-rich soils [62]. This study found that the relative abundance of Chloroflexi decreased significantly with the increase in the amount of biochar combined with phosphorus-containing materials, which might be due to the phosphorus-containing materials. Reducing the soil pH value will inhibit the proliferation of Chloroflexi in low-pH soils, which will reduce the niche of Chloroflexi; Chen et al. [63] also found a similar conclusion. Actinobacteriota is involved in soil nutrient cycling, crop growth, and organic matter degradation [64,65]. Proteobacteria easily survive in nutrient-rich soil environments [38].Therefore, the increase in its relative abundance may be due to the application of biochar to increase the nutrient concentration in soil, which was consistent with the results of Lang et al. [17]. In addition, Proteobacteria contain many heavy metal oxidase gene members related to heavy metal resistance or immobilization, which made it highly tolerant to heavy metal pollution [66]. The decrease in soil DTPA-Cd content after biochar application with phosphorus-containing materials may be related to the increase in the relative abundance of Proteobacteria. Further classification results showed that at the genus level, the microbial community structure changed significantly between different treatments, among which Kaistobacter, Lysobacter, Mermoricola, Anaerolinea, and other beneficial microorganisms were detected with a higher abundance. Compared with CK treatment, the other treatment groups showed new dominant genera, such as Cellvibrio, Actinotalea, Ochrobactrum, and Achromobacter. Related studies have shown that the microbial community structure in soil could reveal the changes in soil environmental factors, especially the impact of soil pollution. The physical and chemical properties of soil are closely related to the concentration of pollutants [67]. Cellvibrio is a kind of Gram-negative bacteria, which is known for its ability to decompose cellulose and plays an important role in the carbon cycle in nature [68]. Ochrobactrum is a kind of bacteria with aerobic denitrification characteristics, which shows strong adaptability in various environments [69]. Studies have shown that there is a significant positive correlation between Ochrobactrum and the content of organic carbon, nitrogen, carboxylic acids, and polymers in soil, which helps to accelerate the metabolic process of complex carbon sources of polymers [70]. Anaerolinea can not only degrade hydrocarbon compounds under anaerobic conditions, but its increase in soil may also promote the degradation of PAHs in sludge [71]. Achromobacter has also been identified as the dominant flora in soil in many studies, and it can be regarded as a potential indicator of soil health or disease [72]. In summary, it was further indicated that the combined application of biochar and phosphorus-containing materials could significantly promote the growth of some soil beneficial bacteria and improve the health status of the soil environment. Among them, T4 treatment had the best effect on the abundance of soil beneficial microbial communities.

5. Conclusions

This study explored the remediation effect of hyperaccumulators on cadmium-contaminated soil under the combined application of biochar and phosphorus-containing materials. The results showed that a single application of biochar could significantly (p < 0.05) increase soil pH and DOC content. Phosphorus-containing materials can significantly (p < 0.05) reduce soil pH; biochar combined with phosphorus-containing materials (T3 and T4 treatment groups) can increase soil DOC content. Biochar and phosphorus-containing materials can reduce the content of Cd and available Cd in soil pore water. Compared with CK treatment, the T4 treatment group has the largest decrease; that is, biochar combined with 2 g/pot phosphorus-containing materials has the best effect on reducing soil pore water and available heavy metals. The combined application of biochar and phosphorus-containing materials could significantly increase the biomass of aboveground and underground parts of amaranth, and significantly increase the activities of catalase and urease in soil. Among them, T4 treatment had the best effect on the biomass increase in aboveground and underground parts, which was 1.64 and 1.71 times those of CK, respectively. T1 had the best effect on soil catalase and urease activity, which were 2.81 and 2.42 times those of CK, respectively. Not only that, the soil microbial community structure has also been improved, and the abundance of beneficial bacteria such as Cellvibrio, Ochrobactrum, and Achromobacter has been improved, thereby improving the environmental function of contaminated soil. It can be seen that biochar combined with phosphorus-containing materials not only effectively compensated for the quality status of phosphorus deficiency and high cadmium in mortar black soil in the Huainan area, but also significantly promoted the growth of hyperaccumulator amaranth. Although the content of Cd in amaranth decreased with the increase in phosphorus-containing materials, the increased biomass greatly increased the total absorption and accumulation of Cd in amaranth, and improved its bioremediation efficiency. Within the scope of this experiment, when the amount of phosphorus-containing material added is 2 g/pot soil, the repair effect is the best.

Author Contributions

Data Curation: Z.J. and Z.Y. Formal Analysis: H.H., D.C. and Z.J. Funding Acquisition: Z.J. Investigation: Z.J., T.W., H.H., M.Z. and W.W. Methodology: Z.J., X.L. and Y.Z. Writing—Original Draft: Y.Z. and Z.J. Writing—Review and Editing: Z.J., Y.Z. All authors have read and agreed to the published version of the manuscript.

Funding

The authors are grateful for the financial support provided by the Key research and development plan of Anhui Province (No. S202104a06020064), The China Geological Survey (Comprehensive Survey of Natural Resources in the Middle Reaches of the Yellow River (Shaanxi Section), Grant No. DD20220868), the Opening Foundation of Anhui Province Engineering Laboratory for Mine Ecological Remediation (No. KS-2022-002), the Opening Foundation of Anhui Green Mine Engineering Research and Development Center in 2022, and the Opening Foundation of Anhui Province Engineering Laboratory of Water and Soil Resources Comprehensive Utilization and Ecological Protection in High Groundwater Mining Area (No. 2022-WSREPMA-05). The authors express their sincere thanks and gratitude to the anonymous reviewers due to their positive comments and constructive suggestions.

Data Availability Statement

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

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The pH value of rhizosphere and non-rhizosphere soil. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error, the same below.
Figure 1. The pH value of rhizosphere and non-rhizosphere soil. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error, the same below.
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Figure 2. DOC value of rhizosphere and non-rhizosphere soil. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
Figure 2. DOC value of rhizosphere and non-rhizosphere soil. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
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Figure 3. Cd concentration in soil pore water changes with time.
Figure 3. Cd concentration in soil pore water changes with time.
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Figure 4. Effects of different treatments on soil available cadmium content. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
Figure 4. Effects of different treatments on soil available cadmium content. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
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Figure 5. Effects of different treatments on soil enzyme activities. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
Figure 5. Effects of different treatments on soil enzyme activities. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
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Figure 6. Effects of different treatments on aboveground and root biomass of amaranth. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
Figure 6. Effects of different treatments on aboveground and root biomass of amaranth. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
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Figure 7. Effects of different treatments on phosphorus uptake by amaranth. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
Figure 7. Effects of different treatments on phosphorus uptake by amaranth. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
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Figure 8. Effects of different treatments on phosphorus accumulation in amaranth. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
Figure 8. Effects of different treatments on phosphorus accumulation in amaranth. Note: Different lowercase letters represent significant differences between the treatment groups (p < 0.05), and the error line represents ± standard error.
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Figure 9. Relative abundance of soil dominant bacteria at phylum level.
Figure 9. Relative abundance of soil dominant bacteria at phylum level.
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Figure 10. Relative abundance of soil dominant bacteria at genus level.
Figure 10. Relative abundance of soil dominant bacteria at genus level.
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Figure 11. A correlation heat map of soil microbial communities (phylum level) with physical and chemical properties and available cadmium content. Note: ** indicates that at the 0.01 level, the correlation is extremely significant; * indicates that at the 0.01 level, the correlation is significant. The same applies below.
Figure 11. A correlation heat map of soil microbial communities (phylum level) with physical and chemical properties and available cadmium content. Note: ** indicates that at the 0.01 level, the correlation is extremely significant; * indicates that at the 0.01 level, the correlation is significant. The same applies below.
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Figure 12. A correlation heat map of soil microbial communities (genus level) with physical and chemical properties and available cadmium content. Note: ** indicates that at the 0.01 level, the correlation is extremely significant; * indicates that at the 0.01 level, the correlation is significant. The same applies below.
Figure 12. A correlation heat map of soil microbial communities (genus level) with physical and chemical properties and available cadmium content. Note: ** indicates that at the 0.01 level, the correlation is extremely significant; * indicates that at the 0.01 level, the correlation is significant. The same applies below.
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Figure 13. RDA analysis of soil microbial community and physicochemical properties and available cadmium content. Note: The blue arrow represents the response variable indicator, and the red arrow represents the explanatory variable indicator.
Figure 13. RDA analysis of soil microbial community and physicochemical properties and available cadmium content. Note: The blue arrow represents the response variable indicator, and the red arrow represents the explanatory variable indicator.
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Figure 14. Changes in Cd content in shoots and roots of amaranth plants with phosphorus content in soil. (a) The change of Cd content in shoot with P content; (b) The change of Cd content in plant roots with P content.
Figure 14. Changes in Cd content in shoots and roots of amaranth plants with phosphorus content in soil. (a) The change of Cd content in shoot with P content; (b) The change of Cd content in plant roots with P content.
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Table 1. Effects of different treatments on Cd uptake by amaranth and soil available Cd.
Table 1. Effects of different treatments on Cd uptake by amaranth and soil available Cd.
TreatmentCd Content (mg·kg−1)Cd Accumulation (μg·pot−1)Available CadmiumBioaccumulation FactorTranslocation Coefficient
ShootRootShootRoot
CK2.02 ± 0.03 a4.75 ± 0.17 a2.81 ± 0.10 c6.02 ± 0.31 c0.85 ± 0.03 a2.130.42
T11.68 ± 0.02 b3.65 ± 0.03 b3.66 ± 0.04 ab6.97 ± 0.16 ab0.81 ± 0.06 b1.770.46
T21.57 ± 0.01 c3.03 ± 0.02 c3.89 ± 0.06 b6.60 ± 0.08 b0.78 ± 0.05 c1.650.51
T31.34 ± 0.01 d2.65 ± 0.05 d3.91 ± 0.11 a7.26 ± 0.19 a0.75 ± 0.05 d1.420.51
T41.07 ± 0.02 e1.94 ± 0.03 e3.90 ± 0.11 ab6.72 ± 0.11 ab0.72 ± 0.04 e1.120.55
Note: Different lowercase letters indicate significant differences between treatment groups (p < 0.05).
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MDPI and ACS Style

Jiang, Z.; Hua, H.; Yin, Z.; Wu, T.; Zhou, Y.; Chen, D.; Li, X.; Zhao, M.; Wang, W. The Combination of Biochar and Phosphorus-Containing Materials Can Effectively Enhance the Remediation Capacity of Amaranth on Cadmium-Contaminated Soil and Improve the Structure of Microbial Communities. Agronomy 2024, 14, 2300. https://doi.org/10.3390/agronomy14102300

AMA Style

Jiang Z, Hua H, Yin Z, Wu T, Zhou Y, Chen D, Li X, Zhao M, Wang W. The Combination of Biochar and Phosphorus-Containing Materials Can Effectively Enhance the Remediation Capacity of Amaranth on Cadmium-Contaminated Soil and Improve the Structure of Microbial Communities. Agronomy. 2024; 14(10):2300. https://doi.org/10.3390/agronomy14102300

Chicago/Turabian Style

Jiang, Zhiyang, Hongmei Hua, Zheng Yin, Tingsen Wu, Yuzhi Zhou, Daokun Chen, Xinbin Li, Mingze Zhao, and Wenshuo Wang. 2024. "The Combination of Biochar and Phosphorus-Containing Materials Can Effectively Enhance the Remediation Capacity of Amaranth on Cadmium-Contaminated Soil and Improve the Structure of Microbial Communities" Agronomy 14, no. 10: 2300. https://doi.org/10.3390/agronomy14102300

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