Co-application of biochar and nitrogen fertilizer promotes rice performance, decreases cadmium availability, and shapes rhizosphere bacterial community in paddy soil☆
Graphical abstract
Introduction
Rice is a crucial staple food that has been extensively cultivated in various areas all over the globe, providing essential nourishment for more than half the population of the world (Carrijo et al., 2017). Nearly one-third of global rice is produced in China (Ye et al., 2012). It is worth noting that there would be a domestic demand of 20% more rice production by 2030 due to the growing population (Faostat, 2019). However, numerous studies have revealed that a large number of agricultural soils have been suffering by Cd contamination, mainly resulting from emissions from surrounding industries and mining activities (Rizwan et al., 2017; Ye et al., 2017). The national survey indicated that the rate of Cd in cultivated soils exceeding the standards in China reached 7.0%, being the highest among heavy metals (Li et al., 2014). Cd is a highly toxic trace element, exerting negative effects on the soil health and development of crops and humans (Vazquez et al., 2020). One particular concern is that Cd affects plant growth, cell division and metabolic activities, resulting in declines in the yield and quality of agricultural crops (Feng et al., 2018). Cd can also reduce the activity of chlorophyll-related enzymes, destroying the structure of chloroplasts, impeding photosynthesis, and then affecting the growth of plants, and in severe case leading to plant death (Rehman et al., 2020). In addition, Cd is easily transferred from soil to the edible parts of rice, wheat and other crops, and eventually entering the human body through the food chain. Reports revealed that excessive Cd has attributed to a series of body organ diseases, which negatively influences functions of lung, brain, kidney and blood circulation (Rana et al., 2018). Research results showed that about 10%–20% of rice and rice products sold in China suffered from heavy metal pollution issues (Zhang et al., 2015b). Thus, it is of substantial significance to remediate Cd contaminated soil and ensure rice safety and productivity.
It is known that nitrogen (N) is a vitally essential nutrient element required for plant growth and productivity (Nishida and Suzaki, 2018). Nowadays, there have been various forms of N fertilizers extensively used in farmland such as amide nitrogen fertilizers, ammonium nitrogen fertilizers and nitrate nitrogen fertilizers, accounting for more than 60% of the total fertilizer consumption in China (Yang et al., 2020). Researches have shown that application of N fertilizers influences the physicochemical properties of soil, affecting the migration of heavy metals and their bioavailability in soil. Besides, N is an important component of amino acids, chlorophyll and protein in plant cells (Daniel-Vedele et al., 2010), effectively regulating the absorption and accumulation of Cd by plants. N in plants can balance heavy metal toxicity through mechanisms at molecular, biochemical, cellular, and whole plant levels (Srivastava et al., 2019). However, an excessive amount of N fertilizers has often been used in intensively cultivated croplands for improving crop yield. Excessive application of N fertilizers is a major contributor for N leaching, NH3 volatilization and losses of nitrogenous gases (Ying et al., 2017). Besides, N fertilizer attributed to soil acidification, which enhanced Cd bioavailability (Zhao et al., 2020). Therefore, the amount of N fertilizer should be controlled and applied appropriately, mitigating the negative impact of excessive nitrogen on the Cd contaminated plant-soil system.
Biochar has gained increasing attention for solving the problem of Cd contamination in soil over the past decades. Biochar is a kind of carbon-rich solid material produced by high-temperature pyrolysis of biomass under oxygen-limited conditions (Ahmad et al., 2014), which possesses various characters such as high alkalinity, large porosity and surface areas, negative surface charge, and many surface functional groups, it could enhance Cd adsorption and decrease Cd plant uptake (Cheng et al., 2019). Moreover, substantial studies showed that biochar consists of various nutrients (such as K, Mg, Na, N, and P), which is of great benefit for plant growth and enhancement of crop yield (Nguyen et al., 2018). For example, Kätterer et al. (2019) set up a 10-year field experiment in a semi-humid area in Kenya and their results showed that the addition of biochar significantly increased the yield of corn and soybeans, improved soil porosity, pH, water retention capacity and enhanced the bioavailability of phosphorus. However, biochar cannot provide sufficient nutrients to the plants, therefore, biochar blended with chemical fertilizer has been come up recently as a better practice to improve the fertilizer utilization rate and crop productivity (Faloye et al., 2019).
Soil microorganisms play a vital role regarding nutrient conversion, crop productivity and heavy metal remediation (Caporale and Violantea, 2016). Soil microorganisms are sensitive to heavy metal stress and are often used to indicate changes in soil environmental quality (Li et al., 2020a, 2020b). Studies have shown that heavy metal pollution can significantly inhibit the growth and reproduction of soil microorganisms, changing the community composition, and reducing community diversity (Haider et al., 2021). Decrease of soil microbial activity caused by heavy metal pollution destroys the nutrient cycle and material decomposition in soils (Huang et al., 2017), influencing soil physicochemical properties (organic matter content, water holding capacity, pH value, etc.), which in turn affects the toxicity and bioavailability of heavy metal (Kenarova et al., 2014; Zhang et al., 2016). Researches have demonstrated that biochar affected community composition of microorganisms (Zhou et al., 2019; Naeem et al., 2021). Biochar can promote the electron transfer between bacteria and heavy metals, thereby promoting the conversion and reducing the toxicity of heavy metals to soil microorganisms (Zhu et al., 2017). Biochar provides important habitat for soil microbes owning to its large surfaces and rich pore structures (Quilliam et al., 2013; Zhu et al., 2017). Study also showed that biochar led to modification of soil microbes involved in elemental cycles (Yang et al., 2016). Additionally, Qiao et al. (2019) demonstrated that N fertilizer could increase the abundance of plant growth-promoting microbes. Though the influences of biochar combined with N fertilizer on the improvement of soil fertility and crop productivity has been reported (Oladele et al., 2019; Lustosa et al., 2020), few studies have been carried out to explore how this combination influence the yield and Cd uptake of rice, variations of soil microorganisms as well as the complicated relationship between Cd transformation and microbe-plant-soil nexus. Therefore, gaining a thorough understanding of the effects of biochar combined with N fertilizer on yield and Cd uptake of rice and microbial properties could provide new insights to assist in improving rice production and guaranteeing food safety.
In this study, a pot experiment was conducted to investigate: (1) the effects of N fertilizer and biochar on the yield and Cd uptake of rice; (2) how do the N fertilizer and biochar treatments shift soil bacteria activity; (3) the response of soil microbial community to changes in Cd availability in soil. We hypothesized that combination of biochar and N fertilizer would alter soil physicochemical properties thus transform the diversity and composition of soil bacterial. We also hypothesized that the alterations in rice yield and Cd uptake correlate to the transformations in soil microbial community.
Section snippets
Experimental materials
In this study, the experimental soil was collected from a paddy field at a depth of 0–20 cm from Xiangtan City (E118 46′, N26 49’), Hunan province, South China, where Cd pollution in agricultural soil has been known for years. The type of soil was acidic red soil. The basic soil properties were: pH 6.2, soil organic matter (SOM) 37.9 g/kg, cation exchange capacity (CEC) 12.36 cmol/kg, total nitrogen (TN) 18.43%, alkaline hydrolysis of nitrogen (AHN) 164.69 mg/kg, available phosphorous (AP)
Influences of BN on rice yield and soil Cd bioavailability
As shown in Fig. 2(a), the rice yield was significantly improved with single N treatments, and increased by 15.8%, 35.9% and 54.4% under the application of N1, N2 and N3, respectively, compared with CK (P < 0.05). Compared to corresponding treatments without biochar, there were increases of 14.3%, 16.0%, 26.7% and 32.2% in yield in the B, BN1, BN2 and BN3 than that of CK and single N1, N2 and N3.
Fig. 1(a) demonstrated that available Cd concentration in soil increased to varying degrees in
Effects of BN on the rice performance
In recent years, the potential impact of soil Cd pollution on safe cultivation and productivity of agricultural crop has attained substantial attention. In this study, pronounced effects of the co-application of biochar and nitrogen fertilizers on rice yield in comparison with sole biochar and nitrogen fertilizers were observed (Fig. 2(a)), which was consensus with report of Rafael et al. (2019) stating that biochar blended with nitrogen fertilizer enhanced biomass yield of crop relative to CK
Conclusions
This study explored the synergistic effect of biochar and nitrogen fertilizer on soil Cd bioavailability, rice yield and soil biochemical properties. The results demonstrated that co-application of BN contributed to decreases in soil Cd availability and Cd uptake of rice. At the same time, BN co-application exerted a better performance on rice yield in comparison with sole N and B. In addition, the results indicated that alterations in soil properties such as soil pH, OM, AHN and available Cd
Author statement
Li Zhang: Data curation, Writing - original draft, Formal analysis. Yulei He: Experiment design, Doing all experiments. Dasong Lin: Supervision, Project administration, Conceptualization, Validation. Yanpo Yao: Reviewing, Visualization. Ningning Song: Reviewing, Visualization. Fangli Wang: Visualization.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Special thanks give to Prof. Liping Weng who contributed greatly to improve the quality of this paper. This work was financially supported by the National Natural Science Foundation of China (41877403).
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This paper has been recommended for acceptance by Yong Sik Ok.
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These two authors contributed equally to this work.