Struvite-supported biochar composite effectively lowers Cu bio-availability and the abundance of antibiotic-resistance genes in soil
Graphical abstract
Introduction
China's pig industry has entered into a fast growth period (Wang et al., 2016b). By the end of 2017, the number of slaughtered fattened pigs in China reached 70,202.1 million heads per year (Statistics, 2018). Meanwhile, massive amounts of pig manure are produced consequently. For integrated nutrient management, pig manure and its derivatives, such as biogas slurry, are extensively used as organic fertilizers in agriculture for their ability to enhance soil fertility and promote crop growth (Guo et al., 2019). However, the long-term application of manure has caused serious environmental problems in agricultural soil, such as pollution with heavy metals and antibiotics (Shi et al., 2019; Tang et al., 2015), increased risk of nitrate and phosphorus leaching (Sørensen and Rubæk, 2012), and rapid emergence of antibiotic resistance in the soil microbiome in particular (Xie et al., 2018). The high prevalence of antibiotic resistant genes (ARGs) in manured agricultural soils has caused worldwide concern (Chee-Sanford et al., 2009; Heuer et al., 2011). In view of the risk of ARG transmission between native biological communities and human pathogens (Fang et al., 2018; Forsberg et al., 2012), strategies to mitigate the dissemination of ARGs in manured soil are of great importance to human health.
Heavy metals and antibiotics as stressors all affect the transferability of soil ARGs, but heavy metals may be more important due to their ability to exert longer-term selective pressure on soil organisms (Knapp et al., 2017; Xu et al., 2017). For example, as a common heavy metal, Cu has been reported to be closely associated with the prevalence of ARGs in manured soils (Ji et al., 2012; Zhu et al., 2013). This may be because the stress of excessive Cu, especially its bio-available species, could select bacterial strains with a higher likelihood of expressing multidrug resistance (Berg et al., 2010). Therefore, with Cu pollution, the acquisition and maintenance of ARGs could be enhanced through the increased cross-resistance and co-resistance among bacterial communities (Gao et al., 2015; Xu et al., 2017).
Some of the available evidence show that reducing the migration activity or bio-availability of heavy metals in the environment could mitigate ARG proliferation. For instance, Li et al. (2017) noted that the addition of biochar could immobilize bio-available Cu and bio-available Zn and decrease their co-selection pressure, thereby partially mitigating the propagation of ARGs during chicken manure composting. Zhang et al. (2018) also suggested that the reduced ARG copies during sludge composting are related to the immobilization of heavy metals by natural zeolite application.
In recent years, our team has developed various magnesium-modified materials and used them for simultaneously recovering N and P nutrients from wastewater and pig slurry (Jing et al., 2019; Wang et al., 2019; Xia et al., 2016). Further studies have confirmed that reusing the recovered struvite-contained products as soil amendments could efficiently immobilize heavy metals and consequently reduce the mobility and bio-availability of heavy metals (Li et al., 2018; Wang et al., 2018; Wang et al., 2016a). As the selective pressure of heavy metals exerted on organisms would decrease with immobilization, the application of the N and P recovery products as amendments could further help mitigate the ARG pollution in manured soil.
This study prepared a struvite-supported biochar composite (MAP/BC) by recovering N and P from pig slurry with Mg(OH)2-modified biochar (Mg(OH)2/BC). MAP/BC was subsequently used as an eco-friendly amendment for in situ remediation of Cu- and ARG-contaminated soil. The simultaneous effects of MAP/BC on Cu immobilization, ARG profiles and soil microbial were explored. The correlations among bio-available Cu (bioCu), ARG abundance, and bacterial composition during soil remediation were also studied. The results will provide insights for the evaluation of the potential for struvite-based nitrogen and phosphorus recovery products.
Section snippets
Preparation of MAP/BC
The preparation procedures of MAP/BC were as follows. First, a pig slurry was filtered with a 0.45 μm acetate fiber membrane filter. The characteristics of the filtered pig slurry are given in Table S1. Second, 0.4 g Mg(OH)2/BC (detailed preparation procedures and micromorphology information are given in Text. S1 and Fig. S1) was added to 1 L of pig slurry, and the mixture was shaken horizontally at 180 rpm on a shaking table for 24 h at 25 °C. Third, the filtered precipitate was washed by
Characterization of MAP/BC
The surface morphological properties and chemical composition of MAP/BC are given in Fig. S2. The SEM images indicated that after the nutrient recovery process, clustered-growing prismatic-shaped crystals mainly comprising Mg, O, N and P were formed (Fig. S3). The XRD patterns showed that the diffraction peaks corresponding to Mg(NH4)PO4·6H2O were identified in MAP/BC. The above results suggest that MAP/BC is a bamboo biochar-based phosphorus-rich material recovered from pig slurry, and the
Conclusion
This study investigated the effects of a nutrient-recovery product MAP/BC on Cu immobilization, ARG composition, and bacterial community in Cu-contaminated agricultural soil. MAP/BC amendment could immobilize Cu through the formation of copper-phosphate precipitation and surface complex. With MAP/BC treatment, the acid-soluble Cu content decreased by 0.47-fold while the residual Cu content increased by 1.41-fold. Moreover, the total abundance of nine target ARGs in Cu-contaminated soil were
CRediT authorship contribution statement
Yuan Li:Conceptualization, Methodology, Software, Visualization, Investigation, Writing - original draft.Xuejiang Wang:Resources, Supervision, Data curation, Project administration, Writing - review & editing.Yuan Wang:Formal analysis, Software.Fei Wang:Software, Writing - review & editing.Siqing Xia:Writing - review & editing.Jianfu Zhao:Resources, Project administration, Supervision, Writing - review & editing.
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.
Acknowledgments
The authors thanks for the support of the National Natural Science Foundation of China (51678421, 41571301, 21777120).
References (49)
- et al.
The role of Cu content on the structural properties and hardness of TiN–Cu nanocomposite film
J. Alloys Compd.
(2017) - et al.
Heavy metal-induced co-selection of antibiotic resistance genes in the gut microbiota of collembolans
Sci. Total Environ.
(2019) - et al.
Dissemination of antibiotic resistance genes and human pathogenic bacteria from a pig feedlot to the surrounding stream and agricultural soils
J. Hazard. Mater.
(2018) - et al.
Does animal manure application improve soil aggregation? Insights from nine long-term fertilization experiments
Sci. Total Environ.
(2019) - et al.
Evolution of corresponding resistance genes in the water of fish tanks with multiple stresses of antibiotics and heavy metals
Water Res.
(2017) - et al.
Antibiotic resistance gene spread due to manure application on agricultural fields
Curr. Opin. Microbiol.
(2011) - et al.
Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China
J. Hazard. Mater.
(2012) - et al.
Effects of bamboo charcoal on antibiotic resistance genes during chicken manure composting
Ecotoxicol. Environ. Saf.
(2017) - et al.
XRD, XPS and SEM characterisation of Cu–NbC nanocomposite produced by mechanical alloying
Mater. Chem. Phys.
(2008) - et al.
Bacterial metal resistance genes and metal bioavailability in contaminated sediments
Environ. Pollut.
(2014)
Mass balance-based inventory of heavy metals inputs to and outputs from agricultural soils in Zhejiang Province, China
Sci. Total Environ.
Effects of different swine manure to wheat straw ratios on antibiotic resistance genes and the microbial community structure during anaerobic digestion
Bioresour. Technol.
Effects of long-term manure applications on the occurrence of antibiotics and antibiotic resistance genes (ARGs) in paddy soils: evidence from four field experiments in south of China
Soil Biol. Biochem.
Integrated analysis on economic and environmental consequences of livestock husbandry on different scale in China
J. Clean. Prod.
Comparison of palygorskite and struvite supported palygorskite derived from phosphate recovery in wastewater for in-situ immobilization of Cu, Pb and Cd in contaminated soil
J. Hazard. Mater.
Struvite crystallization combined adsorption of phosphate and ammonium from aqueous solutions by mesoporous MgO–loaded diatomite
Colloids Surf. A Physicochem. Eng. Asp.
Effect of the selective pressure of sub-lethal level of heavy metals on the fate and distribution of ARGs in the catchment scale
Environ. Pollut.
Occurrence of antibiotic resistance genes in landfill leachate treatment plant and its effluent-receiving soil and surface water
Environ. Pollut.
Impacts of zero valent iron, natural zeolite and Dnase on the fate of antibiotic resistance genes during thermophilic and mesophilic anaerobic digestion of swine manure
Bioresour. Technol.
Nutrients, heavy metals and microbial communities co-driven distribution of antibiotic resistance genes in adjacent environment of mariculture
Environ. Pollut.
Adsorption of Cu (II) and Cd (II) from aqueous solutions by ferromanganese binary oxide–biochar composites
Sci. Total Environ.
Gephi: an open source software for exploring and manipulating networks
Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field
Lett. Appl. Microbiol.
Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay
Environ. Sci. Technol.
Cited by (33)
A review on biochar composites for soil remediation applications: Comprehensive solution to contemporary challenges
2023, Journal of Environmental Chemical EngineeringMechanism for combined application of biochar and Bacillus cereus to reduce antibiotic resistance genes in copper contaminated soil and lettuce
2023, Science of the Total EnvironmentCompetitive adsorption of heavy metals between Ca–P and Mg–P products from wastewater during struvite crystallization
2023, Journal of Environmental ManagementConversion of swine manure into biochar for soil amendment: Efficacy and underlying mechanism of dissipating antibiotic resistance genes
2023, Science of the Total Environment