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. 2023 Mar 28;9(4):e14892. doi: 10.1016/j.heliyon.2023.e14892

Effects of macromolecular organic acids on reducing inorganic phosphorus fixation in soil

Yuwen Shen a,∗, Zheng Ma a,∗∗, Haining Chen b, Haitao Lin a, Guodong Li c, Mingli Li c, Deshui Tan a, Wensheng Gao c, Shuying Jiao d, Ping Liu a, Xiaozong Song a, Shourui Chang e
PMCID: PMC10070650  PMID: 37025842

Abstract

To improve the availability of inorganic phosphorus (P) in soil, we investigated the role of three macromolecular organic acids (MOAs), including fulvic acid (FA), polyaspartic acid (PA), and tannic acid (TA), in reducing the fixation of inorganic P fertilizer in the soil. AlPO4, FePO4, and Ca8H2(PO4)6·5H2O crystals were chosen as insoluble phosphate representatives in the soil to simulate the solubilization process of inorganic P by MOAs. The microstructural and physicochemical properties of AlPO4, FePO4, and Ca8H2(PO4)6·5H2O were determined by scanning electron microscopy (SEM), Fourier-transform infrared spectroscopy (FT-IR), and X-ray photoelectron spectroscopy (XPS) before and after treatment of MOAs. In addition, the amounts of leached P and fixed inorganic P in Inceptisols and Alfisols affected by MOAs combined with superphosphate (SP) fertilizer were determined by soil leaching experiments. The presence of the three MOAs significantly increased the concentration of leached P and reduced the contents of insoluble inorganic phosphate formed with iron, aluminum, and calcium fixed in the soil, in which PA combined with SP had the most significant effect. Furthermore, the less inorganic P fixation in the combination treatment of MOAs and SP resulted in a greater wheat yield and P uptake. Therefore, MOAs could be a synergistic material for increasing P fertilizer utilization.

Keywords: Inorganic phosphorus fixation, Fulvic acid, Polyaspartic acid, Tannic acid, Phosphorus use efficiency

1. Introduction

To increase the yield of crops, farmers often use excessive phosphorus (P) fertilizer in farmland because the utilization rate of P fertilizer has been reported to be as low as 10%–20% in some cases [1]. Most P fertilizers are unavailable to plants due to soil fixation [[2], [3], [4]]. Fe, Al, and Ca oxides/hydroxides are the main soil mineral compounds that decrease the P solubility [[5], [6], [7]], and excess P fertilizer can accumulate in the soil [8]. Resources of phosphate rock minerals are concentrated in a few countries (such as Morocco), resulting in the instability of P fertilizer prices and farmers' anxiety.

Therefore, it is necessary to develop P fertilizers with enhanced efficiency, which can decrease the fixation of P fertilizer, especially the inorganic P fertilizer in the soil. In addition, previous studies have reported that plant roots can secrete low-molecular-weight organic acids (LMWOAs) and solubilize P from soil [9,10]. However, the LMWOAs secreted by the roots are not easy to collect and can be easily degraded in the soil, thus affecting the sustainability of their effects.

Fulvic acid (FA), polyaspartic acid (PA), and tannic acid (TA) represent three types of macromolecular organic acids (MOAs) with carboxyl, amino, and phenolic groups, respectively, as the main functional groups. These three kinds of organic acids are often used to add organic matter to prepare organic-inorganic compound fertilizer.

FA is isolated from lignite, a polyelectrolytic macromolecule originating from the chemical and biological degradation of plant and animal residues and microbial cells [11]. FA is composed of aromatic rings, bridges (such as alkylene, ether, or ester linkages), and side chains (such as alkyl, carboxyl, and hydroxyl groups), with a high abundance of carboxyl groups [12]. As a polymer consisting of free carboxylic and amide groups [13], PA can serve as an organic matter additive in combination with urea [14] to improve nitrogen use efficiency because of its excellent chelating capability, dispersibility, and adsorption. TA is a plant secondary polyphenolic compound. It exists in the bark, fruit, and fallen leaves of many trees (such as oak and lacquer), representing 20%–50% of the composition of leaves and bark of some species [15]. It has been reported that both humic acid (HA) and FA can inhibit the precipitation of P with heavy metals and enhance the P availability to plants [[16], [17], [18]]. Wang et al. [19] have reported that HAs can turn highly insoluble phosphates into highly available P, contributing to plant growth. In 2019, Yang et al. have analyzed the chemical and structural features of phosphate mineral transformation induced by synthetic HA.

The effects of FA, PA, and TA on reducing inorganic P fixation in soil have not been systematically studied. The chemical reactions between FA, PA, or TA and phosphate minerals remain unknown. Therefore, we hypothesized that these organic acids (FA, PA, and TA), in combination with P fertilizer, could reduce P fixation in soil. The reduction of P fixation by MOAs might be attributed to the interactions between carboxyl, amino, or phenolic groups and phosphate minerals. If the hypothesis is verified, we can mix MOAs with inorganic P fertilizer to prepare organic-inorganic compound fertilizer to enhance the utilization rate of P fertilizer. We aimed to investigate 1) the micromorphology and compositional structure of three inorganic phosphate minerals before and after being reacted with MOAs, 2) the effect of MOAs on increasing P concentration in soil leaching solutions and reducing insoluble inorganic P in soils, and 3) the effect of the combination of MOAs and inorganic P fertilizer on crop yield and P uptake, and finally, we explored which type of MOA was more suitable as a phosphate fertilizer synergist.

2. Materials and methods

2.1. Materials

FA was purchased from Shanghai Aladdin Biochemical Technology Co., Ltd. PA powder with a purity of ≥94.00% was kindly provided by Kingenta Ecological Engineering Group Co., which was produced by the thermal condensation catalysis. TA was obtained from Shanghai Sinopharm Reagent Group Co., Ltd. Octacalcium phosphate [Ca8H2(PO4)6·5H2O, Ca8P], iron phosphate (FePO4), and aluminum phosphate (AlPO4), which were used as highly insoluble phosphate representatives in our research, were supplied by Sigma-Aldrich Company.

2.2. Solubilization experiment on phosphate minerals by MOAs

Three phosphate chemicals, FePO4, AlPO4, and Ca8H2(PO4)6··5H2O, were selected to represent Fe–P, Al–P, and Ca8–P, respectively, in the soil to simulate the solubilization process of insoluble inorganic P by MOAs [20]. Briefly, 0.2 g phosphate chemical (Ca8H2(PO4)6··5H2O, FePO4, or AlPO4) was added in a tube containing 5 mL 8 g L−1 MOA (FA, PA or TA) aqueous solution. Phosphate chemical and MOA reacted in pairs for 24 h. The weight ratio of solid MOA and phosphate chemical was 1:5, which is the usual addition ratio to prepare organic-inorganic compound fertilizer. After being centrifugated (3500 r·min−1) for 10 min and filtration of the liquid, the remaining solids were washed with deionized water three times. After further filtration, the remaining solids were placed in the dryer at room temperature for 7 days.

2.3. Structural analysis of phosphate minerals

The microstructures, composition, and physicochemical properties of phosphate minerals, FePO4, AlPO4, and Ca8H2(PO4)6·5H2O with and without reaction with MOAs were determined by the characterization methods as follows [21]. About 0.1 g of phosphate minerals with or without reaction was dried, followed by the morphological observation under an EVO 18 scanning electron microscope (SEM, Zeiss, Germany). X-ray photoelectron spectroscopy (XPS, Thermo Fisher Scientific ESCALAB Xi+) was used to investigate the chemical states of phosphate minerals. Fourier-transform infrared spectroscopy (FT-IR) spectra were recorded on a VERTEX-70/70v FT-IR spectrometer (Bruker Optics, Germany), scanning in the wavenumber range from 400 cm−1 to 4000 cm−1.

2.4. Soil leaching experiment

The soils used in the experiment were obtained from farmland. They were Alfisols derived from acidic magmatite without calcareous sediments (Guan Li Zhen Xiao Chen Jia Cun, Qixia City, Shandong Province, China) and Inceptisols derived from fluvial sediment rich in calcium carbonate (Jiyang Test Station, Jinan, Shandong Province, China). Briefly, arable soil at a depth of 0–20 cm was collected and air-dried. The dried soils were then sieved (<2 mm). Table 1 lists the main physical and chemical properties of the two soils. The organic matter, total P, and available P of soils were determined by the potassium dichromate volumetric method [22], molybdenum antimony anti-colorimetry [22], and the Olsen method. Other basic physical and chemical properties of soils were determined according to the handbook [22]. Freshly incubated soil specimens were blended with water at a ratio of 1:2.5 (w/v, soil to water), followed by vibration for 1 h. The soil pH was assessed using a pH meter (METTLER TOLEDO S210–K pH meter, USA), and the cation exchange capacity (CEC) was determined by the ammonium acetate (1 mol L−1) exchange method.

Table 1.

Basic physical and chemical characteristics of soil.

Soil type Organic matter (g·kg−1) Olsen P (mg·kg−1) Total P (mg·kg−1) pH EC (mS·cm−1) CEC (cmol·kg−1)
Alfisols 9.40 51.30 ± 19.80 263.56 5.60 0.36 14.58
Inceptisols 12.10 28.63 ± 9.80 370.42 7.60 3.43 12.66
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The soil leaching experiments were carried out through a PVC cylindrical pipe with a diameter of 6 cm [23]. A layer of nylon mesh (200 mesh) was placed on the bottom of the pipe to block the soils. Subsequently, 700.00 g of air-dried soil was added to each pipe. There were five treatments, without P fertilizer (CK), with superphosphate (SP, P 19%), SP combined with FA (SP-FA), SP combined with PA (SP-PA), and SP combined with TA (SP-TA). The above-mentioned materials added to the soils were all solid powders. Next, the soil mixtures were loaded into the column, forming a 60-cm high soil column. The P fertilizer added in each treatment was at the same concentration of 12.73 g SP per column, equal to 524 kg P ha−1, and it was about 10 times that used by the farmer in wheat production. For all the treatments with MOAs, the added amounts of HA, PA, and TA were the same as 2.546 g per column. The ratio of SP to MOAs (FA, PA, and TA, respectively) was 1:0.2. Before leaching, 1200 mL deionized water per column was added to saturate the soil. Then the soil columns were incubated at room temperature for 1 day to let the soil fertilizer completely wet. Next, 400 mL H2O was added to the column for the first leaching, and the flow rate was controlled at 2.0 mL per minute by a medical infusion device. The collection of the leaching solution lasted for 24 h. Such leaching procedure was repeated six times on days 2, 9, 16, 23, 30, and 37 of cultivation, and the volume of the leaching solution was measured.

To examine the pH effect on P fixation in soils, the pH of the leaching solution was adjusted from 5 to 9 at 25 ± 0.1 °C using 0.1 mol·L−1 HCl and 0.1 mol·L−1 NaOH solutions. The leaching solution was kept in the column with a constant contact time of 8 h.

2.4.1. Liquid P analysis

The total P in the leaching solution (including not only soluble P but also colloidal and granular P in the solution) was oxidized with potassium persulfate and directly determined by molybdenum blue colorimetry [24]. The water-soluble total P was directly determined by molybdenum blue colorimetry using a 0.45-μm filter membrane and oxidized by potassium persulfate [24]. Molybdate reactive P (MRP) was directly determined by molybdenum blue colorimetry after pressure filtration using a 0.45-μm filter membrane [25].

2.4.2. Soil phosphate fixing analysis

Insoluble inorganic P in soil mainly exists in the form of solid phosphate. It specifically includes aluminum phosphate, occluded phosphate, calcium phosphate, and iron phosphate [26]. The changes in different forms of inorganic P in the soil before and after leaching were detected as follows.

Ca2–P (mainly calcium hydrogen phosphate, CaHPO4·2H2O): Briefly, 1 g of air-dried and sieved (<100 mesh) soil was put into a centrifuge tube, followed by the addition of 50 mL 0.25 mol·L−1 NaHCO3 solution. The mixture was shaken for 1 h (25 °C). After centrifugation (3500 r·min−1) for 8 min, 10 mL of supernatant was collected and placed into a 25-mL volumetric flask. The P concentration in the supernatant was determined by the molybdenum antimony resistance colorimetric method.

Ca8–P (mainly octacalcium phosphate, Ca8H2(PO4)6·5H2O): After being extracted with NaHCO3 solution twice, the soils were washed with 95% alcohol (25 mL per time), and the clear solution after centrifugation was discarded. Next, the soil pellet was resuspended in 50 mL of ammonium acetate solution and allowed to stand for up to 4 h. Subsequently, the samples were centrifuged at 3500 r·min−1 for 8 min, and the P concentration in the supernatant was determined by molybdenum antimony resistance colorimetric method.

Al–P (mainly aluminum phosphate, AlPO4): 1 g of air-dried and sieved (<100 mesh) soil was added into a 100-mL centrifuge tube. The soils were extracted by 1.0 mol L−1 NH4Cl and then extracted by 0.5 mol L−1 NH4F solution at pH 8.2. The mixture was centrifuged after being shaken for 1 h (25 °C). The P concentration in the supernatant was determined by the molybdenum antimony resistance colorimetric method.

Fe–P (mainly Ferric phosphate, FePO4): The soils extracted with Al–P were rinsed two times with saturated NaCl solution and then extracted using 0.1 mol L−1 NaOH solution. The mixture was shaken for 2 h (25 °C), allowed to stand for 16 h, shaken again for 2 h, and centrifuged. The supernatant was put into a triangular flask, 1.5 mL concentrated sulfuric acid was added, and the mixture was allowed to stand overnight. The P concentration in the supernatant was determined by the molybdenum antimony resistance colorimetric method.

O–P (occluded phosphate, mainly P that is difficult to release in the cinnamate lattice): The soils extracted with Fe–P were rinsed two times with saturated NaCl solution. Next, 40 mL of 0.3 mol·L−1 sodium citrate solution was mixed with the soils. The soil blocks were stirred and broken completely, followed by the addition of 1 g sodium dithionite, and the mixture was put into a 90 °C water bath. After the temperature of the solution reached 90 °C, the soils were stirred with an electric mixer for 15 min, followed by the addition of 10 mL of 0.5 mol L−1 NaOH solution. The mixture was stirred for 10 min, cooled, and centrifuged, and the supernatant was collected into a 100-mL volumetric flask. The soils were washed twice with saturated NaCl solution (20 mL per time). The clear solution was transferred into a 100-mL volumetric flask and diluted with deionized water to the volume. Then, 10 mL solution was added into a 50-mL Erlenmeyer flask, followed by the addition of 10 mL of the three-acid mixture (sulfuric acid, nitric acid, and perchloric acid). A small funnel was put on the top of the flask. The flask was heated until perchloric acid and nitric acid were completely decomposed, and the sulfuric acid solution was refluxed. After cooling, a white solid appeared. The white solid was dissolved in 50 mL water and put into a 100-mL volumetric flask. The P concentration of the solution was determined by the molybdenum antimony resistance colorimetric method.

Ca10–P (mainly hydroxyapatite, Ca10(PO4)6·(OH)2): The soil extracted with O–P was mixed with 50 mL of 0.5 mol·L−1 sulfuric acid, and the mixture was shaken for 1 h (25 °C) and then centrifuged. The P concentration of the supernatant was determined by the molybdenum antimony resistance colorimetric method.

2.4.3. Soil enzyme activity analysis

Enzyme activities of soil samples were determined with a 96-well microplate approach as previously described [27]. The activity of alkaline phosphatase (ALP) was measured using disodium phenyl phosphate as a substrate at a wavelength of 660 nm.

2.5. Field experiments of wheat yield and P uptake

Field experiments were carried out to investigate the effects of MOAs on wheat yield and P uptake, and the experimental treatments were the same as those of leaching experiments. The soils were Inceptisols from the Jiyang Test Station, Jinan, Shandong Province, China. Jiyang Test Station was located in the main production area of wheat and corn rotation in China, with a temperate monsoon climate. Each experiment was conducted in triplicate. The area of each plot was 40 m2 (8 m × 5 m), and a 1-m protection line was set outside the plots. The wheat variety was Jimai 22. The seeding rate was 120 kg seed per hectare. The wheat growth time was from October 6th to June 8th of next year. The wheat plants were harvested from a block of 1 m × 1 m. The amounts of N, P, and K nutrients applied in each plot were 240 kg ha−1, 52 kg ha−1, and 75 kg ha−1, respectively. The content of MOAs was 20% of the total fertilizer weight. The fertilizers used in the present analysis included urea (N, 46%), SP (P, 19%), and potassium sulfate (K, 42%), which were supplied by Kinzhengda Corporation. The granular P fertilizer was ground into powder by a crusher and mixed well with the MOA powder. Finally, the mixtures were applied in a depth of 10–15 cm of soil. N and K fertilizers were applied to the soil by a seeder. Wheat was cultivated to maturity, and the yield and P uptake of wheat were calculated at harvest.

2.6. Statistical analysis

Statistical analyses were performed using SPSS 15.0 (Statistical package for social science). The effects of additives on soil physicochemical and microbiological properties were determined using analysis of variance (ANOVA). The differences under various conditions were determined by Duncan's test. P ≤ 0.05 was considered statistically significant. OriginPro 8.5 was adopted to establish the kinetic modeling of the experimental data.

3. Results and discussion

3.1. Structural analysis and physicochemical characteristics of phosphate minerals

Fig. 1a–c shows the surface change of phosphate minerals FePO4, AlPO4, and Ca8H2(PO4)6·5H2O before and after being dissolved by MOAs. Without MOAs, the FePO4 crystal was solid with a smooth surface. After solubilization by FA and PA, many holes appeared on the surface of FePO4. However, TA treatment resulted in a complete disintegration of FePO4 into numerous flakes of particles, which had loose and irregular-like structures. SEM image of the AlPO4 mineral showed an ordered lamellar structure. After solubilization by FA and PA, only their layered structure became loose, and there was no significant structural change. After TA solubilization, the surface of the AlPO4 layered structure became very smooth and even reconstituted a spherical surface. We also studied the solubilization of MOAs on Ca8H2(PO4)6·5H2O solid surface (Fig. 1c). However, Ca8H2(PO4)6·5H2O itself had a loose structure, and its surface was full of holes. After MOAs were added, the solid surface had no noticeable change. In terms of the structures of the three inorganic phosphate solids, FePO4 was a smooth and solid crystal, AlPO4 had an intercalated layer structure, and the surface of Ca8H2(PO4)6·5H2O was pitted. According to the morphology of the three crystals, FePO4 was the most difficult to be dissolved by MOAs.

Fig. 1.

Fig. 1

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Change of SEM micrography of (a) FePO4 and FePO4 dissolved by FA, PA, and TA, (b) AlPO4 and AlPO4 dissolved by FA, PA, and TA, and (c) Ca8H2(PO4)6·5H2O (Ca8–P) and Ca8–P dissolved by FA, PA, and TA.

The FT-IR and XPS data (Fig. 2, Fig. 3) showed that there was strong chemical interaction between MOAs and the formation of new mineral species. Fig. 2a illustrates the FT-IR spectra of FePO4 dissolved by FA, PA, and TA. The appearance of a broad absorption peak at 3450 cm−1 in FePO4-FA and FePO4-TA plots belonged to the O–H stretching vibration of the intermolecular hydrogen bond. Absorption at frequencies near below 3000 cm−1 belonged to the C–H stretching vibration of saturated hydrocarbon in FePO4-FA and FePO4-TA plots. The absorption peak in the FePO4-TA plot at 1750 cm−1 and 1320 cm−1 belonged to C Created by potrace 1.16, written by Peter Selinger 2001-2019 O and C–O, respectively. These findings indicated the strong chemical interactions between FePO4 and MOAs. Therefore, we hypothesized that the interaction between FePO4 and TA was the strongest. Fig. 2b reveals that the introduced functional groups of AlPO4 after MOAs solubilization were basically the same as those of FePO4, while the interaction between FePO4 and TA was the strongest. Fig. 2c shows that after MOA solubilization, only the C–H stretching vibration peak of saturated hydrocarbon near below 3000 cm−1 could be observed. It seemed that MOAs also had a chemical reaction with Ca8H2(PO4)6·5H2O.

Fig. 2.

Fig. 2

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FT-IR spectra of (a) FePO4, (b) AlPO4, and (c) Ca8H2(PO4)6·5H2O (Ca8P) before and after dissolved by FA, PA, and TA.

Fig. 3.

Fig. 3

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Change of (a) Fe 2p, (b) P 2p, (c) Al 2p, and (d) P 2p of FePO4 and AlPO4 before and after being dissolved by FA), PA, and TA.

XPS data in Fig. 3a clearly showed a parallel reduction of Fe from +3 to +2 [21] after being dissolved by MOAs. Those data indicated that the dissolution of the FePO4 was induced by MOAs via a redox process, especially by the solubilization of TA (Fig. 3a and b). Indeed, the polyphenols are highly redox-active, and this redox strength can result in an efficient metamorphosis of the FePO4 minerals. Fig. 3c and d show a significant change in the XPS peak morphology of AlPO4 minerals. At the interface between PA and AlPO4, the Al signal was not even collected, implying an obvious chemical reaction between AlPO4 and MOAs, especially between AlPO4 and PA.

In previous studies, the carboxyl, amino, and phenolic groups can complex ions into stable compounds and keep P ions in an exchangeable state, leading to improved availability of P [4,28,29]. This process can prevent P and metal elements in the soil from forming AlPO4, FePO4, and Calcium phosphate, which are more difficult for plants to absorb [30]. According to our structural analysis, the three MOAs could not only change the microstructure of insoluble inorganic P phosphate but also interact with them to make them more soluble by forming complexes with Fe, Al, and Ca.

3.2. Impact of MOAs on P leaching content

The addition of MOAs significantly increased the leaching amount of P through the soil leaching experiment (Fig. 4a–c). The total P release rate in the Inceptisols was ranked as follows: SP-PA > SP-TA > SP-FA > SP, while such order in the Alfisols became SP-PA > SP-FA > SP-TA > SP. Compared with the SP treatment, the P release rate in the SP-PA treatment was increased from 15.15% to 32.90% (in Inceptisols) and from 13.25% to 28.49% (in Alfisols). The changing trends of dissolved total P (DTP) and MRP contents in the leaching solution were basically consistent with those of the P release rate. The amount of DTP was generally higher compared with MRP, showing that DTP contained a small part of organic P.

Fig. 4.

Fig. 4

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Effects of SP, SP-FA, SP-PA, and SP-TA treatments on (a) the total P release rate, (b) DTP content, and (c) MRP content in the leaching solution from Inceptisols and Alfisols, respectively. Error bars indicate the standard deviation of four independent replicates, n = 4.

The leaching amounts of three forms of P in all SP-FA treatments were higher in Alfisols compared with Inceptisols. In other treatments, the leaching amounts of different forms of P in Inceptisols were higher compared with Alfisols. In the acid Alfisols, P interacted with Fe and Al efficiently to form insoluble phosphate. Fe and Al, as well as their hydrated oxides, had strong adsorption on P. In Inceptisols, P was mostly fixed in the form of calcium phosphate. After adding FA, the leaching P in Alfisols was generally higher than that in Inceptisols, indicating that FA was much easier to combine with Fe and Al to release P. Besides, the pH of the FA solid was 9.37. The release of P in soil could also be caused by the ion exchange between OH− in solution and phosphate in Fe and Al phosphate complex [31]. PA and TA preferred to release P by binding with Ca. The pH value of the TA solid was 3.13. The acidic microenvironment can dissolve some phosphate bound with Ca [31]. In conclusion, the addition of MOAs could effectively decrease the fixation of P fertilizer in the soil. Moreover, FA was more suitable for Alfisols, while TA and PA should be used in Inceptisols.

The pH value of the leaching solution has an important impact on the P retention capacity of the soil, thus affecting the migration and leaching of soil P [32]. The effect of different pH values of leaching solution on P release in the soil is mainly realized by affecting the occurrence form of P in aqueous solution and the interaction between soil and phosphate. In Fig. 5, after the inorganic acid-based leaching solution at pH 5, 8, and 9 entered into Inceptisols, the pH value of the leaching solution was 7–8, and the soil pH was maintained at about 7.6–7.7. The pH of the soil was not changed significantly after leaching with inorganic leaching solution at pH 5, 8, and 9, and the impact of the leaching solution was within the buffer range of the soil. However, the inorganic pH leaching solution still had an impact on the release of soil P. Within the pH range of 5–9, the leaching amount of DTP in all P fertilizers with MOA treatments was significantly higher compared with the SP treatment. In SP treatment, the change in pH value had no significant effect on the leaching amount of water-soluble P. It showed that leaching inorganic acid or alkali solution had no significant impact on P release without changing the pH value of Inceptisol. After MOAs were added, the leached amount of DTP was increased by 220%–320% compared with the SP treatment. It indicated that although there was no change in soil pH, the addition of MOAs had a complexing reaction with Fe, Al, and Ca insoluble phosphate, increasing P release [33]. The amount of DTP in the SP-FA treatment was increased with the pH value of leaching solutions. The SP-TA treatment displayed an opposite changing trend, while SP-PA treatments had no significant change in the pH value of the leaching solution. The original pH of FA, PA, and TA in solid was 9.37, 7.22, and 3.13, respectively. It showed that the complexing reaction between FA and insoluble phosphate minerals was more robust in the alkaline microenvironment. However, in the acidic microenvironment, the complexing reaction between TA and insoluble phosphate minerals was stronger. For PA, the pH value of the microenvironment had little effect on it. Therefore, to ensure the impact of activating P, we need to consider the microenvironment pH when FA and TA were combined with P fertilizer.

Fig. 5.

Fig. 5

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pH effect of SP, SP-FA, SP-PA, and SP-TA treatments on DTP content in the leaching solution from Inceptisols. Error bars indicate the standard deviation of four independent replicates, n = 4.

3.3. Impact of MOAs on inorganic P fixation in the soil

Fig. 6 a-b shows the contents of different forms of inorganic P in Inceptisols and Alfisols after leaching. According to the existing method, only the concentrations of Al–P, Fe–P, O–P, and Ca–P can be determined in the acid Alfisols. Therefore, the concentrations of Ca2–P, Ca8–P, and Ca10–P were obtained only in alkaline Inceptisols by further classification of Ca–P.

Fig. 6.

Fig. 6

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Effects of without P fertilizer (CK), SP, SP-FA, SP-PA, and SP-TA treatments on inorganic phosphate content in (a) Inceptisols and (b) Alfisols. Error bars indicate the standard deviation of four independent replicates, n = 4.

In general, no matter what treatment, the amount of inorganic P fixed in Alfisols was higher than in Inceptisols. A large amount of P was washed away by water, especially in the treatments containing MOAs. In the absence of exogenous P fertilizer, the primary forms of fixed inorganic P in Inceptisols (Fig. 6a) were Ca10–P and O–P, accounting for 46.15% and 37.09% of the total fixed inorganic P, respectively, and the contents of Fe–P and Al–P were very low. The fixed inorganic P with the highest concentrations in Alfisols (Fig. 6b) were O–P and Ca–P. After the P fertilizer (SP treatment) was added, the main forms of fixed inorganic P in Inceptisols were still Ca10–P and O–P, and the proportions were decreased to 28.55% and 17.88%, respectively. The proportions of fixed Al–P, Fe–P, and Ca8–P in Inceptisols were significantly increased from 3.97%, 3.16%, and 4.52%–17.52%, 15.81%, and 17.30%, respectively. The fixed inorganic P with the highest concentration in Alfisols (Fig. 6b) was O–P, probably due to the less amount of Ca in Alfisols.

In the presence of MOAs, the proportions of fixed Al–P, Fe–P, and Ca8–P in Inceptisols (Fig. 6a) were significantly lower compared with the SP treatment, while the content of Ca2–P was considerably higher compared with the SP treatment. This finding indicated that the combined application of MOAs and P fertilizer significantly reduced the contents of fixed Al–P, Fe–P, and Ca8–P, which were probably transformed into Ca2–P in Inceptisols. At the end of the soil leaching experiment, the content of the single form of soil inorganic P was still dominated by Ca10–P and O–P. The addition of MOAs could reduce the contents of Ca10–P and O–P, while the proportions of Ca10–P and O–P in soil inorganic phosphate were still the highest. It demonstrated again that these two forms were stable and belonged to the main inorganic P fixation source [34]. In Alfisols (Fig. 6b), when P fertilizer was combined with PA, it could most effectively reduce the fixed inorganic P contents in soil. When FA or TA was combined with P fertilizer, the effect of reducing inorganic P fixation was not obvious.

3.4. Soil enzyme activities affected by MOAs

Soil phosphatase can transform P from non-available, organically bound forms into phosphate ions that can be absorbed by microorganisms and plants [35]. The existence of phosphate can inhibit the activity of phosphatase [36]. In Fig. 7, the ALP in Inceptisols was significantly decreased with the addition of P or P fertilizer combined with MOAs. In the early stage of the soil leaching experiment, the ALP activity in soil containing MOAs was substantially lower compared with the treatment only with P fertilizer. The lowest urease activity was found in the SP-PA treatment. It indicated that a higher amount of available P exited in Inceptisols because of the interaction between P fertilizer and MOAs. At the later stage of the soil leaching experiment, the ALP activity in P fertilizer with MOA treatments was increased, which should be caused by the loss of phosphate during the leaching process. In summary, compared with P fertilizer alone treatment, MOAs could increase the amount of active phosphate, and P fertilizer with PA was the best choice for reducing inorganic P fixation in Inceptisols.

Fig. 7.

Fig. 7

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The effects of MOAs on soil ALP activity during the soil leaching experiment in Inceptisols. Error bars are the standard deviation of four independent experiments, n = 4.

3.5. Yield and P uptake of wheat

We studied the effect of MOAs in combination with P fertilizer on wheat yield and P uptake in a field plot experiment. SP-PA and SP-TA treatments remarkably elevated the yield of wheat compared with the treatment only with P fertilizer (Fig. 8a). The P uptake of wheat was ranked as follows: SP-PA > SP-TA > SP-FA > SP > CK (Fig. 8b). With the addition of MOAs in combination with SP, the P uptake by wheat was greater than that of the P fertilizer treatment only, suggesting that the MOAs could not only reduce P fixation in soil but also enhance the absorption of P nutrients by crops. Taken together, these findings implied the potential use of MOAs as synergists to improve the utilization of P fertilizer.

Fig. 8.

Fig. 8

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Effects of without P fertilizer (CK), SP, SP-FA, SP-PA, and SP-TA treatments on the production (a) and P uptake (b) by wheat in Inceptisols. Error bars indicate the standard deviation of three independent replicates, n = 3.

4. Conclusions

We demonstrated that three MOAs (FA, PA, and TA) could reduce inorganic P fixation in soil. AlPO4, FePO4, and Ca8H2(PO4)6·5H2O, which were selected as inorganic phosphate minerals, could react with MOAs and form new complexes that were more available in the soil. Compared with P fertilizer alone, the three MOAs could significantly improve the P release rate and reduce inorganic P fixation in the soil during soil leaching experiments. The complexing reaction between FA and insoluble phosphate minerals was more robust in the alkaline microenvironment. In the acidic microenvironment, the complexing reaction between TA and insoluble phosphate minerals was stronger. For PA, the pH value of the microenvironment had little effect on it. Therefore, to ensure the impact of activating P, we need to consider the microenvironment pH when FA and TA were combined with P fertilizer. The plot experiment further demonstrated that compared with SP alone, the combined application of MOAs and SP could significantly improve the yield and P uptake of wheat, and the combination of PA and SP had the best result, especially in Inceptisols, while SP-FA treatment was more suitable for Alfisols. Therefore, MOAs could serve as potent P fertilizer synergists to enhance P utilization.

Funding

This work was financially supported by the National Natural Science Foundation of China, China (41877100); Major Science and Technology Innovation Projects in Shandong Province, China (2021CXGC010802); Taishan Industry-leading Talent Project, China (LJNY202026); the Innovation Project of Agricultural Science and Technology in Shandong Academy of Agricultural Sciences, China (CXGC2016A07); Shandong Natural Science Foundation (ZR2020MD105); National Key Research and Development Plan, China (2021YFD1901003).

Author contribution statement

Yuwen Shen and Zheng Ma: Conceived and designed the experiments.

Yuwen Shen, Haining Chen, Haitao Lin and Deshui Tan: Performed the experiments.

Yuwen Shen, Guodong Li, Mingli Li, Deshui Tan, and Wensheng Gao: Analyzed and interpreted the data.

Yuwen Shen, Shuying Jiao, Ping Liu, Xiaozong Song and Shourui Chang: Contributed reagents, materials, analysis tools or data.

Yuwen Shen and Zheng Ma: Wrote the paper.

Data availability statement

Data included in article/supp. material/referenced in article.

Declaration of interest’s statement

The authors declare no competing interests.

Additional information

No additional information is available for this paper.

Contributor Information

Yuwen Shen, Email: wendy_yws@163.com.

Zheng Ma, Email: mazheng15@163.com.

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