Acidic conditions enhance the removal of sulfonamide antibiotics and antibiotic resistance determinants in swine manure☆
Graphical abstract
Introduction
Land application of manure is a necessary component of ecological recycling agriculture, which offers many advantages. Nonetheless, the associated ecological risks should not be ignored, such as the environmental contaminants contained in animal feces. Sulfonamide antibiotics (SAs) are frequently used in pig farms to treat diseases and promote growth; however, this also results in large quantities of potentially harmful compounds in excrements, either as metabolites or parent compounds (Boxall et al., 2003). SAs have been reported in manure and manure-derived products at a ppm level (Martínez-Carballo et al., 2007; Qian et al., 2016a), which may delay the establishment of thermophilic temperatures during manure composting (Lin et al., 2016) and inhibit biogas production during anaerobic digestion of manure (Yang et al., 2019). Long-term exposure to antibiotics also induces the accumulation and proliferation of antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) in manure wherein sulfonamide resistance genes could be detected at high abundances (Qian et al., 2016b; Zhu et al., 2013). These antibiotic residues and ARGs/hosts in manure could further be transferred to soils, surface water, underground water, and crops after land application (Hu et al., 2010), which may accelerate the emergence and spread of antibiotic resistance in the environment and ultimately threatens human and animal health.
Both governments and individuals have recognized the need for treating manure prior to land application as a fertilizer to minimize antibiotic resistance contaminants. Traditionally, manure treatment processes are designed to reduce waste volume or otherwise convert it to useful products such as fertilizer and biogas (Van Epps and Blaney, 2016). These manure treatments such as composting, anaerobic digestion, drying, and storage do contribute to the reduction of antibiotic residues by biotic and abiotic transformation, dilution, and adsorption, and also to minimize the dissemination of ARB and ARGs (Gou et al., 2018; Pruden et al., 2013; Van Epps and Blaney, 2016; Zhang et al., 2019b). However, low treatment efficiencies were observed for some antibiotics, including SAs (Spielmeyer, 2018; Zhang et al., 2019b). It is also common to find ARG accumulation in manure after manure management processes including composting (Storteboom et al., 2007; Zhu et al., 2013). Nowadays, manure management processes are expected to become more versatile and could be effectively used to minimize contaminants. Thus, the optimization of manure treatment to effectively remove potentially harmful antibiotics and ARGs is critical. Increased management of manure compost piles such as turning and aeration have been applied to promote antibiotic degradation but is not very effective (Van Epps and Blaney, 2016). Low-cost additives such as biochar (Cui et al., 2016), clay (Awasthi et al., 2019) and sawdust (Zhang et al., 2019c) have been proven to promote antibiotic and ARG removal efficiencies during manure treatment. Nevertheless, it is necessary to continue exploring different manure treatment strategies to develop more cost-efficient and effective options for reducing antibiotic residues.
The initial pH of manure before being subjected to conventional manure management practices is often variable and largely depends on the characteristics of manure itself and also on the additive contents. The pH of aqueous solutions has been demonstrated to influence the hydrolysis (Yang et al., 2009) and photodegradation (Wu et al., 2019) of antibiotics. The effect of pH on antibiotic fates in solid matrices could be different from those observed in aqueous solution, given that biodegradation is often the main mechanism of SAs removal in solid matrixes, including manure (Choi et al., 2016; Yang et al., 2016). Given the simplicity and high operational feasibility of manure pH regulation, this study investigated the possibility of enhancing antibiotic removal in manure via pH optimization and to elucidate the effects of these measures on ARB and ARG abundances as well as the bacterial community structure.
Section snippets
Raw manure and experimental design
Fresh swine manure was collected from a manure storage tank of a livestock farm in Yiwu, China, which contained manure from pigs of different ages and breeds. Prior to incubation, the raw manure sample had a water content of 68.1%, a pH of 7.4, and electrical conductivity of 3.1 mS cm−1 pH adjustments of manure samples were carried out by drop-wise additions of a 10 M sulfuric acid solution into containers with 200 g raw manure under constant stirring and cooling. Manure was sampled at
The dissipation of sulfonamide antibiotics
Only four SAs were detected in the raw manure sample of this work, including SDZ, SDM, SMM, and SMZ (Fig. 1). The residual antibiotics profile of manure reflected the antibiotic usage habits in the livestock industry during pig feeding, and our data partly implied the high use of SAs on the farm. Without pH adjustment, SAs in manure also underwent degradation after a 5-day incubation period, exhibiting an overall SA removal rate of 56.8%. Low treatment efficiencies (i.e., approximately 26–35%)
Conclusion
Adjusting the pH of manure to provide acidic conditions facilitated the removal of sulfonamide antibiotics and sul genes while potentially restricting SRB proliferation and intI1 accumulation. The improved reductions in antibiotics and antibiotic resistance determinants were demonstrated to be closely linked to the pH-induced enrichment of the Firmicutes, which potentially encompass SA-degrading bacteria. This study offers a novel, simple, and effective approach to mitigate antibiotics in
CRediT authorship contribution statement
Hui Lin: Conceptualization, Investigation, Writing - original draft. Wanchun Sun: Investigation. Qiaogang Yu: Validation, Writing - review & editing. Junwei Ma: Supervision, Funding acquisition.
Declaration of interests
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
We would like to thank Prof. Jing Ye from Zhejiang Academy of Agricultural Sciences who assisted with the project administration, sampling, and basic physicochemical analysis and Dr. Xin Zhang from Zhejiang A & F University for her valuable advice on this study as well as her editing of the manuscript. This work was supported by the Zhejiang Provincial Natural Science Foundation of China [grant number LY19D010011] and the National Natural Science Foundation of China [grant numbers 31672234,
References (39)
- et al.
Application of metagenomic analysis for detection of the reduction in the antibiotic resistance genes (ARGs) by the addition of clay during poultry manure composting
Chemosphere
(2019) - et al.
The sorption and transport of a sulphonamide antibiotic in soil systems
Toxicol. Lett.
(2002) - et al.
Prioritisation of veterinary medicines in the UK environment
Toxicol. Lett.
(2003) - et al.
Fate of sulfonamide resistance genes during sludge anaerobic fermentation: roles of sludge components and fermentation pHs
Bioresour. Technol.
(2019) - et al.
Removal characteristics and mechanism of antibiotics using constructed wetlands
Ecol. Eng.
(2016) - et al.
Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting
Bioresour. Technol.
(2016) - et al.
Aerobic composting reduces antibiotic resistance genes in cattle manure and the resistome dissemination in agricultural soils
Sci. Total Environ.
(2018) - et al.
Occurrence and source analysis of typical veterinary antibiotics in manure, soil, vegetables and groundwater from organic vegetable bases, northern China
Environ. Pollut.
(2010) - et al.
Effect of organic carbon and pH on soil sorption of sulfamethazine
Chemosphere
(2009) - et al.
Manure digestate storage under different conditions: chemical characteristics and contaminant residuals
Sci. Total Environ.
(2018)
Effect of temperature on sulfonamide antibiotics degradation, and on antibiotic resistance determinants and hosts in animal manures
Sci. Total Environ.
Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria
Environ. Pollut.
Identification of dominant sulfamethoxazole-degraders in pig farm-impacted soil by DNA and protein stable isotope probing
Environ. Int.
Occurrence of trace elements and antibiotics in manure-based fertilizers from the Zhejiang Province of China
Sci. Total Environ.
Variable effects of oxytetracycline on antibiotic resistance gene abundance and the bacterial community during aerobic composting of cow manure
J. Hazard Mater.
Fate of tetracyclines in swine manure of three selected swine farms in China
J. Environ. Sci.
Occurrence and fate of antibiotics in manure during manure treatments: a short review
Sustain. Chem. Pharm.
Biodegradation of sulfonamide antibiotics in sludge
Chemosphere
Enhanced removal of pharmaceuticals in a biofilter: effects of manipulating co-degradation by carbon feeding
Chemosphere
Cited by (45)
UV-aging reduces the effects of biodegradable microplastics on soil sulfamethoxazole degradation and sul genes development
2025, Journal of Environmental Sciences (China)Vermicompost: In situ retardant of antibiotic resistome accumulation in cropland soils
2024, Journal of Environmental Sciences (China)Co-metabolism driven sulfaquinoxaline removal in microbial electrolysis cells: A mechanistic analysis based on DFT calculation, metabolic pathway and functional enzyme activity
2024, Journal of Environmental Chemical EngineeringInsights into the pH-dependent interactions of sulfadiazine antibiotic with soil particle models
2024, Science of the Total Environment
- ☆
This paper has been recommended for acceptance by Klaus Kümmerer.