Abstract
The effects of long-term biochar application on soil phosphorus (P) flux across the root-soil interface and its availability in the rhizosphere of rice (Oryza sativa L) remain unclear. We used diffusive gradients in thin films (DGT), laser ablation-inductively coupled plasma mass spectrometry, and planar optode sensor techniques to characterize, in-situ, the 2D heterogeneity and dynamics of rhizosphere soil P, iron (Fe), sulfur (S) and trace element fluxes, dissolved oxygen and pH in paddy soil, after 10 years of biochar application. Compared to the control (no biochar applied), biochar applied at 4.5, 22.5 and 45.0 Mg ha−1 yr−1 decreased rhizospheric P fluxes by 11.6%, 63.4% and 79.0%, respectively. This decrease under biochar treatments was attributed to changed redox status of Fe and S caused by the lower dissolved oxygen in rhizosphere soil and increased soil pH induced precipitating of soluble inorganic P into insoluble P forms, such as calcium-bound and residual P that are unavailable for crop uptake. Higher application rate of biochar resulted in lower As and Pb fluxes in rice rhizosphere and their availabilities for crop uptake. The in-situ observation results in rice rhizosphere at μm-scale after 10 years of biochar addition directly showed the complex effects of long-term biochar and rhizosphere heterogeneity on P transformation process.
Graphical Abstract
Highlights
In-situ 2D imaging of rice rhizosphere P, Fe, S, and trace elements was elucidated.
Long-term biochar application conspicuously lowered rice rhizosphere available P.
Soil P release process was related to Fe and S redox status.
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1 Introduction
Production of biochar from crop residues is an important method of agricultural waste management, and biochar application to agricultural land helps increase soil organic matter and nutrients availability such as nitrogen and phosphorus (P) for crop uptake (Wang et al. 2023; Pan et al. 2021). The efficacy of biochar application in soil P availability had more pronounced beneficial effects observed in short-term pot or incubation experiments, contrasting with weakened effects in long-term field conditions (Gao et al. 2019; Glaser and Lehr 2019). Previous studies are more focused on the bulk soil, while biochar-root interaction in the rhizosphere zone has often been neglected, despite it being the most active and dynamic region of nutrient cycling and an important source and sink of P for crop and soils (Apori et al. 2021; Shen et al. 2011). Assessment of rhizosphere P cycling is thus needed for in-depth understanding on how biochar influences nutrient availability for crop uptake.
The rice rhizosphere emerges as a pivotal zone for soil P transformation and crop P uptake. Therefore, it is important to investigate the availability of P in the soil within the rhizosphere, as it directly influences the release process of P in this zone. The complexity and heterogeneity of the rhizosphere environment induced by the release of root exudates, root release of oxygen and rhizosphere microbial activity have potential implications for soil P availability (Yin et al. 2020; Wei et al. 2019). The fluctuation in oxygen levels significantly affects soil P cycling, and the radial oxygen loss is conducive to the changes in the microscale redox potential (Larsen et al. 2015), which further change soil P availability. The migration and transformation of soil P are mainly controlled by its interaction with elements like iron (Fe) and sulfur (S) and arsenic (As) in flooded paddy soils. These interactions occur mainly in the rhizosphere zone where the redox potential of Fe and S undergo changes due to the utilization of dissolved oxygen (DO) during the decomposition of organic matter (Li et al. 2021), influence adsorption and fixation of P and make it less accessible for uptake by plants (Weihrauch and Opp 2018). The dissolution of P from Fe(III)-bound P is a primary source of available P in flooded paddy soils (Khan et al. 2019; Maranguit et al. 2017; Zhang et al. 2003), which might be via the sulfide-induced reduction of Fe(III) hydroxide and direct microbial Fe(III) reduction (Brodersen et al. 2017). Moreover, the speciation and concentration of As is influenced by the extent of Fe(III) reduction and competitive adsorption with P (Deng et al. 2020). In a flooded paddy soil with a high microbial Fe reduction potential, microbial sulfate reduction decreased As mobilization by its precipitation or sorption with FeS minerals (Xu et al. 2019), and the variations in interactions between Fe and P triggered by fluctuations of redox conditions and root activities, which further explains solute release patterns/mechanisms (Fang et al. 2021a). Furthermore, apart from the interaction of soil P with these elements, lower soil pH in rice rhizosphere plays a crucial role in increasing soil P mobilization by the dissolution of calcium phosphate (Brodersen et al. 2017; Marschner et al. 2011).
The distribution of P in rice rhizosphere is heterogeneous on the millimeter scale (Larsen et al. 2015). Challenges in precisely assessing this process in the rhizosphere have been attributed to sampling and interpretative constraints. Traditional rhizosphere research methods including soil shaking, root rinsing, and root bag approaches involve destructive sampling, and low-resolution of nutrient cycling quantification (Kreuzeder et al. 2018; Brodersen et al. 2017). To address these challenges, the diffusive gradients in thin films (DGT) method, characterized by its in-situ, high-resolution, and multi-parameter features based on simple diffusion principles, offers a promising solution (Yin et al. 2020; Williams et al. 2014). The utilization of this methodology by Fang et al. (2021a, b) revealed that rice rhizosphere P depletion facilitated phosphatase activities and mineralization of organic P, which further contributed to a deeper comprehension of P cycle in paddy soils. Our recent research on rice rhizosphere soil P and Fe distribution also demonstrated the successful application of DGT technique in studying nutrient cycling in the paddy soil (Wang et al. 2021a, b; Wang et al. 2019). However, to achieve a comprehensive understanding, concurrently measurement of labile P flux and key factors influencing P release from rhizosphere soil becomes imperative.
The addition of biochar generally improves soil P availability. This improvement primarily stems from the dissolution of P from the biochar material, the increased reduction and dissolution of P in Fe(III) hydroxide, and mineralization of soil organic P by promoting the activities of microorganisms or phosphatase (Eltohamy et al. 2023; Yang et al. 2021; Zhou et al. 2020). However, the conflicting results could potentially be caused by the immobilization of P through the adsorption or precipitation (Yang et al. 2019; Chintala et al. 2014) caused by an elevation in soil pH and crop uptake (Xu et al. 2016). Moreover, the impact of biochar on soil P availability varies depending on the timeframe since its application; the effect is large in the short-term (< 1 year) pot or incubation experiments but weakens in the long-term (> 1 year) field conditions (Gao et al. 2019; Glaser and Lehr 2019). A four-year-long field study in paddy field illustrated that the effectiveness of biochar in increasing soil P availability decreased with the increase in application rate and time (Jiang et al. 2021). It will thus be valuable to understand the mechanism of long-term biochar effects on soil P availability. Notably, prior studies have tended to focus more on soil processes and less on rhizosphere processes. In our investigation using the DGT technique, we discovered a significant reduction in rice rhizosphere available P after 9 years of biochar addition in the field (Chen et al. 2022). However, the lack of available data on long-term effects of biochar on nutrient cycling, particularly in the rhizosphere zone, has been limiting our ability to include biochar amendment as one of the best management practices on a broad scale across the globe (Wei et al. 2019).
Herein, based on previous study, the present study employed a combined in-situ high-resolution approach to delve deeply into the effects of 10 years of continuous biochar application on the bioavailability of soil P, elucidating the key processes influencing P release in the rhizosphere zone of rice, by using a pot experiment. The main hypotheses of this research include: 1) the application of biochar can change the availability of P, Fe, S and trace elements in the rhizosphere of rice; and 2) biochar application affects Fe and S cycles through altering DO and pH, and thereby changing the P availability in the rice rhizosphere soil. The results provide intuitive information on rhizosphere microscale for the sustainable utilization of agricultural waste resources.
2 Materials and methods
2.1 Soil and biochar
The soil was obtained from the upper 20 cm of soil profile in an agricultural land, where biochar had been applied continuously at different rates for 10 years in a rice–wheat cropping experiment, at the Yixing Agro-Environment Research Base of the National Agroecosystem Observatory and Research Station of Changshu (YX, 119°54′E, 31°16′N). The field experiment had four treatments: 1) no biochar applied (control, CK); 2) biochar applied at 0.1% of soil weight (0.1BC, 4.5 Mg ha−1 yr−1); 3) biochar applied at 0.5% of soil weight (0.5BC, 22.5 Mg ha−1 yr−1); and 4) biochar applied at 1.0% of soil weight (1.0BC, 45.0 Mg ha−1 yr−1). In all treatments, the chemical P fertilizers were added at 60 kg P2O5 ha−1 in each season. The urea and potassium chloride (KCl) application dozes were 250 kg N ha−1 (in a ratio of 3:4:3 at basal, tillering, and jointing stages) and 60 kg K2O ha−1, respectively. Detailed information on biochar, soil and fertilization methods used in the field experiment can be found in Chen et al. (2022). The biochar used in the field was derived from rice straw and produced through pyrolysis at a temperature of 500 °C for 8 h, with a heating rate of 5 °C min−1. It was then thoroughly mixed with the top 0–20 cm layer of soil. The properties of biochar were as follows: pH 9.16, total organic carbon and nitrogen concentrations of 620 and 13.3 g kg−1, the cation exchange capacity of 18.9 cmol kg−1, and the concentrations of Ca, P, K, Na, Mg, Fe, Mn, Cu and Zn extracted by Mehlich III which were 2.63, 1.06, 18.43, 3.94, 1.41, 0.01, 0.55, 0.0016 and 0.05 g kg−1, respectively. Soil samples were collected from three random points within each plot using an auger after wheat harvest, and then was composited for each plot. Each soil sample was mixed well and processed separately by removing stones and visible roots, air-drying, and sieving through a 2 mm mesh. A portion of the processed soil was used to characterize soil basic properties and the remaining soil was used in a pot experiment. Soil Olsen-P concentrations were 32.4, 25.9, 29.3 and 37.0 mg kg−1, for the CK, 0.1BC, 0.5BC and 1.0BC treatments, respectively.
2.2 Greenhouse experiment
A greenhouse experiment was conducted using rice seedlings in custom-designed Perspex rhizoboxes from July 27 to August 26, 2020. Each rhizobox had dimensions of 10 × 8 × 20 cm3 and included a detachable plate. The soil used in the experiment was collected and processed separately for each plot in the field experiment. A total of 1 kg (oven-dry equivalent) of air-dry soil was filled into each rhizobox after pre-incubation at 70% water-holding capacity for one week. Rice seedlings were produced in a nursery. Two 10-day-old rice seedlings with a pruned root length of 1.5 cm were transplanted to each rhizobox near the detachable plate. To prevent light penetration into the soil and roots, the rhizoboxes were wrapped with tin foil and kept inclined at 30° angle, allowing the roots to grow along the side of the detachable plate. After transplanting the rice seedlings, nitrogen and potassium fertilizers were added to the soil. Base fertilizers consisted of 0.200 g urea kg−1 soil and 0.175 g KCl kg−1 soil. Two weeks after transplanting, a topdressing of 0.100 g urea kg−1 soil was applied. The soils were flooded with 3 to 5 cm of water covering the soil surface during the whole experiment.
2.3 Planar optode sensor imaging
Soil pH and DO concentrations in the soil solution were measured using a planar optode sensor (PO2100, EasySensor Ltd. Nanjing, China) 14 and 28 days after transplanting. Refer to Supporting Information Text S1 for detailed procedural steps.
2.4 Zr-oxide DGT imaging
Horizontal and vertical distributions of soil DGT-labile P around root tips were visualized on a submillimeter scale using a Zr-oxide DGT (EasySensor Ltd. Nanjing, China) 14 and 28 days after seedling transplanting. Refer to Supporting Information Text S2 for detailed procedural steps. The scheme of experimental design is shown in Fig. S1.
2.5 HR-ZCA DGT imaging
The fluxes of sulfides, metallic cations and oxyanions (P, S, Fe, As, Pb, Co, Ni, Cu and Zn) in the rhizosphere soil were determined after 30 days of transplanting, using HR-ZCA DGT imaging (EasySensor Ltd. Nanjing, China) followed by laser ablation-inductively coupled plasma mass spectrometry (LA-ICP-MS, Agilent Technologies 7700, USA). Refer to Supporting Information Text S3 for detailed procedural steps.
2.6 Soil P fractionation
Soil P fractions were analyzed on samples collected 30 days after transplanting of seedlings following the Tiessen method (Tiessen and Moir 1993). Refer to Supporting Information Text S4 for detailed procedural steps.
2.7 Data analysis
The 2D imaging for measuring the DO concentration, soil pH and selected elements in the rhizosphere was mapped using the Origin software. The association among the elements studied under different biochar application rates was explored through principal component analysis (PCA) by Origin software. Pearson correlation analysis exploring the linear relationship between the selected elements was presented as correlation diagram performed through R version 3.6.1.
3 Results and discussion
3.1 Distribution and dynamics of labile P, DO and pH in rhizosphere
The 2D imaging of the soil rhizosphere P flux illustrated an obvious P depletion area around root tips regardless of the treatment, with the low DGT-P flux corresponding to the area of soil P depletion; the P depletion area gradually expanded with the rice growth as shown from the measurements made 14 and 28 days after the transplanting of seedlings (Fig. S2). High heterogeneity of the localized rhizosphere environment indicated the variations induced by the roots of rice seedlings under different treatments (Fig. S2). The longest root length and total root length were highest in 0.5BC treatment (Table S1). In contrast to previous ex-situ studies by Jin et al. (2019), this study with in-situ high-resolution imaging demonstrated that biochar application reduced P availability in rice rhizosphere soil. Compared with CK treatment, P flux was decreased by 11.6%, 63.4% and 79.0% under the 0.1BC, 0.5BC and 1.0BC treatments, respectively (Fig. S3). The 2D imaging of DO and soil pH also showed highly heterogeneous effects of the treatments in the rhizosphere (Fig. S2). Oxygen secretion was observed along all visible roots and increased over time. The amount of DO increased towards the root tips which corresponds to the increase in root density and greater accumulation of oxygen from root respiration. Labile P decreased with increasing biochar application rate on both measurement times, indicating a negative impact of biochar on rhizospheric P flux.
To further elucidate the correlations, labile P and DO measurements at the same position (2 × 4 cm2) were compared and the average values of unit resolution in the vertical direction for 14th and 28th day measurement were calculated (Fig. 1). The P depletion area around root was positively related with the area of high DO. Consistent with previous studies, soil labile P had the lowest flux when DO concentration was the highest, which indicated the primary effect of root oxygen secretion and nutrient uptake process (Fang et al. 2021a; Williams et al. 2014). In the vertical profile, labile P flux showed a narrower horizontal spread in the treatments with higher rate of biochar application on 14th and 28th days of measurement (Fig. 1c and 1d). Labile P flux and DO had a negative relationship across all treatments. The correlation was gradually weakened along the rate of biochar application. The root-regulated variation of soil pH was weaker than that of labile P, regardless of the treatment and time of measurement (Fig. 2a and b). Soil pH was significantly increased with increasing biochar application rate. The vertical distribution profile of labile P plotted against soil pH (Fig. 2c and d) showed a weak correlation regardless of treatment and time of measurement, unlike its strong negative correlation with DO.
The difference in labile P flux along the vertical axis in the rhizosphere across all the treatments can be attributed to plant uptake of labile P, microbial immobilization and the adsorption of P by Fe plaques on the root surface (Fang et al. 2021a). The oxygen secreted by roots induces changes in redox conditions of the soil solution in the rhizosphere that further affects soil P availability for plant uptake and microbial metabolism (Larsen et al. 2015). Under anaerobic condition (i.e. low DO), bacterial demand for P decreases, and the activity of Fe-reducing bacteria increases to enhance labile P flux in rice rhizosphere (McRose and Newman 2021; Wang et al. 2021a, b ). The fluctuation of redox potential affects the release process of P through Fe cycle (Yuan et al. 2021, 2020). Since the region of redox fluctuation is narrower than that of P diffusion around root surfaces, the labile P flux gradient among the treatments was associated with plant uptake of labile P and the formation of Fe plaques on root surfaces (Fang et al. 2021a). Additionally, the fact that root uptake of labile P by mass flow occurs faster than the rate of labile P diffusion from soil solution to rhizosphere (Khan et al. 2019), suggesting that plant uptake of labile P was the main driving factor for the reduction of soil available P in the rhizosphere.
The high specific surface area of biochar, along with presence of alkaline cations (Ca2+ and Mg2+, for instance) in biochar promoted the adsorption and precipitation of soil P (Ghodszad et al. 2022, 2021), thereby reducing soil P availability. The P fraction data showed that Ca-P and residual P increased with the increasing biochar application rate (Fig. S4). The biochar used in this study was pyrolyzed at high temperature (500 °C) and contained a high amount of Ca2+ and Mg2+ ions, which significantly contributed to the adsorption of P (Borno et al. 2018; Ngatia et al. 2017). The adsorption of P on biochar surface occurs by the exchange between solution anions of P and oxidizing functional groups present on biochar surfaces (Chintala et al. 2014). Yang and Lu (2022) have shown that the effect of biochar addition on P availability varied with growth stages of rice that were linked to variations in soil pH and crop uptake of P. In this study, biochar application resulted in an increase in soil pH, which might affect soil P availability through biogeochemical processes, including adsorption–desorption, dissolution, precipitation and complexation (Eduah et al. 2019). However, as soil pH was not strongly affected by biochar application rates, labile P flux was more linked to the change in crop uptake of P and soil DO.
3.2 Distribution of and relationships between labile P, Fe, S and trace elements in rice rhizosphere
Consistent with previous findings (Fang et al. 2021bb; Yin et al. 2020; Williams et al. 2014), rice roots substantially affected the availability of P, Fe and S (Fig. 3). Two possible reasons for the heterogeneity of distribution of these elements in the rhizosphere on the vertical axis are the variation in adsorption and secretion of these elements by rice roots, and the drastic change in physicochemical conditions in the microenvironment of the rice rhizosphere. The decrease in P and Fe flux was expanded further away from the root surface (Fig. 3). This indicates that the effect of Fe plaque formation on rice root surface (Fig. S6) was caused by root oxygen secretion on rhizosphere P adsorption and fixation (Wang et al. 2019). Furthermore, the presence of Fe plaques on root surfaces might be the main factor contributing to the decrease in fluxes of As and Pb in rice rhizosphere, as a significant positive relationship was observed between them (Fig. 4a and b). In contrast to previous findings (Fang et al. 2021b; Yin et al. 2020; Williams et al. 2014), no apical Fe flux hotspots were observed in our study (Fig. 3). This might be owing to the fact that oxidative immobilization of Fe by root oxygen secretion was stronger than the reductive dissolution of Fe by Fe-reducing bacteria activity. Moreover, the spatial patterns of labile P and trace elements (As, Pb, Co, Ni, Cu and Zn) in rhizosphere were congruent with root distribution (Fig. 3 and S5). The average flux of S, labile P and trace elements including Fe, As and Pb was lower in rice rhizosphere compared to bulk soil, and was generally decreased by the application of biochar. Biochar played a significant role in affecting the intensity of trace element fluxes but did not exhibit any patterns in their spatial distribution. Among the trace elements studied, substantial As flux was observed in the rhizosphere but not in bulk soil, while Co and Ni fluxes were lower in rhizosphere compared to bulk soil, and increased with higher rates of biochar application (Fig. S5). Unlike Co, the flux of Cu was greater in the rhizosphere compared to the bulk soil zone (Fig. S5).
The results of PCA highlight distinct differences in flux characteristics among the treatments (Fig. 4a). Soil Fe, S, As and Pb had significantly positive relationships with P (p < 0.01) (Fig. 4b), of which the strongest positive relationship was between P and Fe (correlations coefficients of 0.87, p < 0.001) and the next between P and S (correlations coefficients of 0.69, p < 0.001; Fig. 4c), further emphasizing the importance of Fe and S cycles in soil P mobilization. The microbial and chemical process-mediated Fe(III) reduction in anaerobic conditions of paddy soil enhanced the desorption and dissolution of P from Fe(III) hydroxide (Khan et al. 2019). The significant linear correlation between dissolved sulfide and labile P indicated that the migration of P is mainly regulated by reduction and dissolution of Fe(III)-bound P triggered by sulfide and the mineralization of organic carbon related to sulfate reduction (Wu et al. 2019). The Fe(III) hydroxide and sulfate are reduced to Fe(II) and S(-II) under flooded anaerobic conditions. Biochar application has been shown to promote Fe(III) hydroxide and sulfate reduction by increasing soil organic carbon content (Rajendran et al. 2019). Biochar can also act as an electron shuttle, promoting microbial reduction of Fe(III) (Kappler et al. 2014). In our study, the decrease in labile S(-II) flux may be attributed to the formation of S(-II) precipitates by sulfate reduction, which further affects the adsorption of soil phosphate. Additionally, the formation of Fe(II) phosphate under reducing conditions also resulted in a decrease in soil P availability (Wu et al. 2021). The biogeochemical processes of elements like Fe and S can regulate the change of redox activity regulated by the roots of rice in flooded conditions. These biogeochemical processes play a crucial role in regulating soil P availability in rice rhizosphere under variable rates of biochar application. Therefore, this supports our second hypothesis that biochar application affects Fe and S cycles by altering DO and pH, subsequently influencing soil P bioavailability in rice rhizosphere.
The fluxes of Cu and Ni were significantly negatively correlated with S(-II) in the rhizosphere. The increase in their flux in the rhizosphere was due to S oxidation (Kreuzeder et al. 2018). Under reducing conditions, the formation of sulfide precipitate (such as CuS) may also reduce their fluxes. Significant negative correlations of Cu and Ni with Fe (Fig. 4b) indicate that the adsorption of Cu and Ni by roots was impacted by the formation of Fe plaques on root surfaces, as Fe plaques act as a barrier for their adsorption. A coupling-decoupling phenomenon between Ni and Fe at different positions was found in the rhizosphere of aquatic plants (Li et al. 2022). Root-induced oxidation and acidification in soil solution can improve the availability of Ni, however, the formation of Fe plaque resulting from oxidation may reduce Ni mobility through adsorption. Moreover, a clear relationship among Co, Ni, Cu and Zn was observed by PCA, highlighting the crucial role of biochar in influencing trace element availabilities (Figs. 4a and 5). These findings were similar to the results of previous study that used different DGT substrates in determining the availability of trace elements (Yin et al. 2020).
4 Conclusion
Here, we clarified how to reduce P availability in the rhizosphere zone after 10 years of biochar application on paddy soil. We attribute these findings to DO-derived morphological changes of redox-active elements (Fe and S) and pH-triggered transformation of Ca-P and residual P. The spatial distribution similarity of P, Fe and S proves evidence that variation in root-mediated redox-active element morphology regulates P transformation and release processes in paddy soil. The consistency of chemical flux in spatial distribution characteristics and its difference under biochar addition directly illustrate the complexity of how biochar affects the interaction among elements. Combined with our previous research results, biochar not only increased soil Ca-P but also promoted the hydrolysis of organic P due to the stimulation of phosphatase activity, which eventually could maintain soil available P at sufficient level for crop uptake. Therefore, biochar can be regarded as a slow-release P fertilizer due to its sustained-release effect on soil P by affecting biochemical processes related to P transformation. However, it is crucial to note that a high biochar application rate may lead to soil P accumulation due to the elevated P content in biochar. The ability to adjust the biochar application rate and chemical P fertilizer becomes imperative in addressing this issue. This will help us further realize and utilize biochar resource more efficiently in agricultural eco-system.
Availability of data and materials
The data generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.
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This work was funded by the Natural Science Foundation of Jiangsu Province (BK20230049), the National Natural Science Foundation of China (No. 42277026), the Jiangsu Agricultural Science and Technology Innovation Fund (CX(22) 3200), and Jiangsu Modern Agricultural Machinery Equipment and Technology Demonstration Promotion Project (NJ2023-29).
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jiahui Yuan, Hao Chen and Guanglei Chen. The first draft of the manuscript was written by Jiahui Yuan and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Yuan, J., Chen, H., Chen, G. et al. Long-term biochar application influences phosphorus and associated iron and sulfur transformations in the rhizosphere. Carbon Res. 3, 25 (2024). https://doi.org/10.1007/s44246-024-00109-0
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DOI: https://doi.org/10.1007/s44246-024-00109-0