Coupling amendment of biochar and organic fertilizers increases maize yield and phosphorus uptake by regulating soil phosphatase activity and phosphorus-acquiring microbiota

Highlights

• Long-term biochar and organic fertilizer inputs affected soil P pool and maize growth.

• Biochar and organic fertilizer increased 12–23% labile-P but reduced 13–19% stable-P.

• Biochar and organic fertilizer enhanced soil P-cycling enzyme activity and gene abundance.

• Organically-amended increase in maize productivity relied on microbial-driven P dynamics.

Abstract

Biochar and organic fertilizers are important alternatives to mineral fertilizers. Thus, it is important to understand how the co-application of biochar and organic fertilizers influences crop productivity and soil-plant phosphorus (P) trade-offs. Herein, we conducted a field fertilization experiment for eight years with maize-cabbage rotation. This experiment contained five treatments: no fertilization (CK), mineral fertilizers (CF), CF + biochar (BF), 20% substitution of mineral nitrogen (N) with organic fertilizers (OF), and OF + biochar (BOF). The fertilization regimes of all plots were maintained since 2013. The results showed that soil P pool composition but not P bioavailability differed significantly between the five treatments. Compared with the CF treatment, soil labile-P content in the BF, OF, and BOF treatments significantly increased by 12–23% and soil stable-P content decreased by 13–19%. Besides, the soil moderately labile-P content in the OF and BOF significantly decreased by 40% and 10% and increased by 31% in the BF as compared to the CF. The activities of soil acid (ACP) and alkaline phosphatase (ALP) in the BF, OF, and BOF significantly increased by 8–44% and 16–49% respectively compared to the CK. Furthermore, the abundance of P-acquiring genes (bpp, phoD, phoX, ppx, ppk, and phnK) in the BF, OF, and BOF increased by 22–114% compared to the CK. Plant P uptake and maize yield were significantly correlated with soil ACP and ALP activities as well as the abundance of phnK, ppx, phoD, phoX, and pqqC genes but not to the contents of soil P components. In conclusion, the co-application of biochar and organic fertilizer on maize productivity increases was mainly related to the improvement of soil phosphatase activity and P-acquiring gene abundance.

Introduction

Maize (Zea mays L.) is an important food crop and it plays an important role in food and energy security (Zhang et al., 2018). Maize crops require a high resource input to attain a high crop yield (Dowswell, 2019). However, long-term superfluous application of chemical fertilizers could reduce nutrient utilization rate and productivity of maize crops (Zhang et al., 2021). Recently, the replacement of chemical fertilizers with organic fertilizers or biochar addition has become a common management practice for improving soil fertility and crop productivity (Sandhu et al., 2019, Arif et al., 2021, Peng et al., 2021). In addition, biochar and organic fertilizer could improve soil aggregate stability, reduce nutrient losses, and increase soil carbon (C) and phosphorus (P) bioavailability (Zhang et al., 2021, Arif et al., 2021, Yuan et al., 2022). These evidences indicate that the co-applications of biochar and organic fertilizers have the potential effectively improving maize productivity and utilization of soil P. However, the underlying mechanism of the co-application of biochar with an organic fertilizer in improving maize productivity and soil P availability remains unclear. This gap further limits the understanding of the roles of soil P pools and transformations in crop productivity.

After the application of mineral P fertilizer to croplands, the mobility of P in the soil decreases rapidly in a short time, resulting in P and metal cations precipitation or deposition in organic matter pools (Karunanithi et al., 2015). Biochar is a C source generated via pyrolysis of biomass under a high temperature and oxygen-limiting condition, and its application enhances P release in the soil (Yang et al., 2021). Oxides or carbonates in biochar could replace P, increasing P retention in the soil and reducing P losses due to leaching and runoff (Madiba et al., 2016, Wang et al., 2022a). Additionally, biochar has a huge surface area and rich porous structure that could effectively improve the soil environment, provide good living conditions for soil microorganisms, and promote microbe-driven transformations of soil P (Yang et al., 2020, Wang et al., 2022a).

Organic fertilizer, a soil improvement material, itself contains a large amount of organic matter, metabolites, and microorganisms, which could improve the recovery of soil nutrients and contribute to the dissolution and absorption of P by plants (Luo et al., 2019, Mahmood et al., 2017). Under the context of organic amendment combined with biochar, the biochar stabilizes organic C in organic fertilizer and maintains the nutrient supply in the soil (Arif et al., 2021). Previous studies have shown that organic materials including biochar and manure could promote the growth of P-solubilizing microbiome and enhance their functions in the soil (Xu et al., 2019, Bi et al., 2020). Functional microbes could activate and increase soil P availability by solubilizing and mineralizing soil legacy P such as organic P, which further enhances plant P uptake (Alori et al., 2017). Thus, high maize productivity and P efficient use could be related to the microbe-driven transformations between soil P components and available P mining.

Based on the stability or availability, the P fractions in soil can be split into three categories, namely labile-P, moderately labile-P, and stable P components (Mahmood et al., 2021). Out of these P fractions, plants can more rapidly assimilate and utilize soil labile P. The moderately labile-P is easily converted to labile-P through soil organic matter mineralization and the stable-P is fixed via the soil medium and plants couldn’t utilize the P directly (Niederberger et al., 2019). According to the biological process (Wu et al., 2020), soil bioavailable P pool could be divided into four categories, namely CaCl₂-P, enzyme-P, citrate-P, and HCl-P.

Soil microorganisms and crop roots secrete phosphatases and other substances or metabolites, which could activate the soil to utilize difficult-to-use P components and convert them into available P for crop uptake (Bünemann et al., 2012, Luo et al., 2017, Luo et al., 2019). The phoD- and phoX-harboring guilds are known microbial taxa encoding phosphatases for organic P mineralization (Luo et al., 2020). Soil P-solubilizing taxa also could exude organic acids and other substances to dissolve moderately labile- or stable-P fractions for crop uptake (Richardson and Simpson, 2011). The pyrroloquinoline quinone encoded by the pqqC gene dissolving inorganic phosphate promotes a phosphorolytic microbes that dissolves insoluble P into water-soluble inorganic P (Rodríguez et al., 2006). Thus, determining the composition and bioavailable components of soil P pools and P-acquiring microbiota could provide better insight into the co-application control of biochar and organic fertilizers on the P trade-offs of soils and plants.

The objective of this study was to examine the co-application effects of biochar and organic fertilizers on soil P pool composition, soil P bioavailability, and microbe-driven dynamics of soil P using a long-term field experiment (started in 2013). Soil P fractions were divided into different categories according to their characteristic and availability. The activities of extracellular phosphatase and the abundances of P-acquiring microbial populations were employed to explore the microbe-driven P dynamics in soil. Quantitative PCR was used to characterize the abundance of the target genes in connection with organic P mineralization (bpp, phoD, and phoX), inorganic P dissolution (ppx, ppk, and pqqC), and phosphonate transportation in microbial cells (phnK) (Table 1). Meanwhile, we also explored the correlations of plant P uptake and maize yield with soil P pool composition, P bioavailability, and microbe-driven P dynamics. We hypothesized that the co-applications of biochar and organic fertilizers led to increased maize productivity that was related to microbe-mediated transformations between soil P components and available P mining.