Changes in bacterial community structure and antibiotic resistance genes in soil in the vicinity of a pharmaceutical factory☆
Introduction
Total annual antibiotic use, including those associated with medical and veterinary applications, has reached 100,000–200,000 t worldwide (Wang and Tang, 2010). China is the largest producer and consumer of antibiotics in the world (Hvistendahl, 2012). In 2013, antibiotic usage reached approximately 162,000 t in China, of which 77,760 and 84,240 t were consumed by humans and animals, respectively (Zhang et al., 2015). More than 150 antibiotics are in use today (von Nussbaum et al., 2006), and these include fluoroquinolones, macrolides, tetracyclines, and sulfonamides, which are commonly used in human and veterinary medicine (Giger et al., 2003, Golet et al., 2003).
Given that significant amounts of antibiotics are produced and subsequently released into different environmental constituents such as soil and surface and ground water (Andreozzi et al., 2004, Bartelt-Hunt et al., 2011, Boxall et al., 2004), the potential impact of antibiotic residues on various organisms is currently an important focus of research. Soil contains millions of microbes per gram (Torsvik et al., 1990), which play a fundamental role in soil functions such as element cycling, environmental pollutant degradation, and energy flow (Barros and Feijoo, 2003, Bremner and Blackmer, 1978, Lewis et al., 1999). Antibiotic residues in soil will greatly change bacterial community structures, and thus disturb soil functions (Fang et al., 2016, Pinna et al., 2012, Zhang et al., 2017). Understanding the fate and transport of antibiotics in the environment is fundamental to limit their spread and optimize their management. Antibiotics can enter the environment through different pathways. Adsorption was considered the major process that governs the mobility and transport of antibiotics in the environment, and bound-residue formation largely controls the long-term storage of antibiotics in soils and sediments (Carstens et al., 2013). Adsorption can be a limiting factor for the subsurface horizon transport and biodegradation of antibiotics by soil microorganisms and can also prevent antibiotics from undergoing biotic and abiotic degradation (Vasudevan et al., 2009). Antibiotics can also be released into the environment through the air and water near production sites. Pharmaceutical factories, in most cases, are not capable of completely removing these compounds from their wastewater (Gadipelly et al., 2014), which could contaminate the surrounding environment.
Antibiotics might not only disrupt the functions of soil microbial communities and possibly affect their growth, but also lead to the spread of antibiotic resistance genes (ARGs) (Zhu et al., 2013). The migration and transformation of ARGs in the soil environment is potentially more harmful than the occurrence of antibiotic residues in the environment (Arias and Murray, 2009, Ji et al., 2012, Perreten and Boerlin, 2003). Even at levels below the clinically determined minimum inhibitory concentrations, some antibiotics can stimulate the emergence of bacteria harboring ARGs (Jechalke et al., 2014). Horizontal gene transfer (HGT) is considered the main mechanism of ARG propagation (Thomas and Nielsen, 2005). Some ARGs have been shown to exist in transposons, integrons, or plasmids, which are mobilizable elements that can be transferred among bacteria (Martinez et al., 2007).
In this study, the soil in the vicinity of a pharmaceutical factory that had produced antibiotics for years, was collected to study soil chemical characteristics, bacterial community structure, ARG distribution, and the relationships among these parameters. The purpose of this study was to investigate the bacterial community structure changes the occurrence and distribution of ARGs based on distance from the factory and soil depth. To our best knowledge, this is the first study to investigate the occurrence and distribution of antibiotic resistance genes in soil in the vicinity of a pharmaceutical factory.
Section snippets
Sampling sites
Soil sampling was conducted in November 2016 from various locations in the vicinity of a pharmaceutical factory in Shangyu, Zhejiang Province, China; the manufacture of bulk pharmaceutical chemicals is the principal business of this factory, and most of these are quinolones such as ofloxacin, levofloxacin, gatifloxacin, and ciprofloxacin. The annual yield of quinolones for this factory reaches 2900 t, and it has manufactured antibiotics for 12 years (up to soil sample collection). In addition,
Soil chemical characteristics and detection of antibiotics
The chemical properties of each soil sample are provided in Table 1; the average TC, TN, TS, aK, aP, and SOM contents in each soil group were 9.70–27.68 g/kg, 0.36–2.04 g/kg, 0.05–0.26 g/kg, 68.43–110.10 g/kg, 3.42–8.80 mg/kg, and 5.71–25.96 g/kg, respectively. The amounts of these soil nutrients were similar in soil samples at a depth of 10 cm, except for the TS in the Z10 sample and aK in the H10 and S10 samples, which were higher than other samples. However, at a depth of 30 cm, these
Conclusion
This study reveals bacterial changes and the occurrence of ARGs in the vicinity of a pharmaceutical factory to evaluate the risk of antibiotic production processes on environmental health. Results of alpha indices showed that soil microbial diversity and evenness were not significantly changed. However, results from PCoA suggested that primary genera in soil were significantly altered. Further RDA analysis revealed that soil nutrients were important in shaping the bacterial community structure.
Acknowledgment
This work was financially supported by the National Key Research and Development Program of China (2017YFD0200503), and the Natural Science Foundation of China (21577128, 21777144).
References (57)
- et al.
A combined mass and energy balance to provide bioindicators of soil microbiological quality
Biophys. Chem.
(2003) - et al.
Occurrence of steroid hormones and antibiotics in shallow groundwater impacted by livestock waste control facilities
J. Contam. Hydrol.
(2011) 16S metagenomics reveals changes in the soil bacterial community driven by soil organic C, N-fertilizer and tillage-crop residue management
Soil Tillage Res.
(2016)- et al.
Changes in soil microbial community structure and function associated with degradation and resistance of carbendazim and chlortetracycline during repeated treatments
Sci. Total Environ.
(2016) - et al.
Soil urease activity and bacterial ureC gene copy numbers: effect of pH
Geoderma
(2017) - et al.
Fate and effects of veterinary antibiotics in soil
Trends Microbiol.
(2014) - 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.
Biotic and abiotic degradation of four cephalosporin antibiotics in a lake surface water and sediment
Chemosphere
(2010) - et al.
Rapid residue analysis of fluoroquinolones in raw bovine milk by online solid phase extraction followed by liquid chromatography coupled to tandem mass spectrometry
J. Chromatogr. A.
(2011) - et al.
Community structure and elevational distribution pattern of soil Actinobacteria in alpine grasslands
Acta Ecol. Sin.
(2017)
Bacterial community structure and its relationship to soil physico-chemical characteristics in alder stands with different management histories
Ecol. Eng.
Simultaneous determination of most prescribed antibiotics in multiple urban wastewater by SPE-LC-MS/MS
J. Chromatogr. B.
Veterinary antibiotics at environmentally relevant concentrations inhibit soil iron reduction and nitrification
Soil Biol. Biochem.
pH-dependent ciprofloxacin sorption to soils: interaction mechanisms and soil factors influencing sorption
Geoderma
Quantitative analysis of multiple illicit drugs in preserved oral fluid by solid-phase extraction and liquid chromatography-tandem mass spectrometry
Forensic Sci. Int.
Changes in antibiotic concentrations and antibiotic resistome during commercial composting of animal manures
Environ. Pollut.
Alterations in soil microbial communities caused by treatments with penicillin or neomycin
Environ. Sci. Pollut. Res. Int.
Antibiotics in the environment: Occurrence in Italian STPs, fate, and preliminary assessment on algal toxicity of amoxicillin
Environ. Sci. Technol.
Antibiotic-resistant bugs in the 21st century -- a clinical super-challenge
N. Engl. J. Med.
Livestock antibiotic effects on nitrification, denitrification, and microbial community composition in soils
Open J. Soil Sci.
Veterinary medicines in the environment
Rev. Environ. Contam. Toxicol.
Determination of nitrogen in soil by the Kjeldahl method
J. Agric. Sci.
Nitrous oxide: emission from soils during nitrification of fertilizer nitrogen
Science
First evidence for the presence of a hydrogenase in the sulfur-reducing bacterium Desulfuromonas acetoxidans
J. Bacteriol.
Sorption and photodegradation processes govern distribution and fate of sulfamethazine in freshwater-sediment microcosms
Environ. Sci. Technol.
Spatial distribution of soil nutrients after the establishment of sand-fixing shrubs on sand dune
Plant Soil Environ.
Pharmaceutical industry wastewater: review of the technologies for water treatment and reuse
Ind. Eng. Chem. Res.
Occurrence and fate of antibiotics as trace contaminants in wastewaters, sewage sludges, and surface waters
Chimia
Cited by (16)
Seasonal dissemination of antibiotic resistome from livestock farms to surrounding soil and air: Bacterial hosts and risks for human exposure
2023, Journal of Environmental ManagementCitation Excerpt :The co-occurrence modes in the soils showed that intI1 was only correlated with Roseburia and Turicibacter. The spread of ARGs in soil was related to its potential hosts, and the reproduction of most bacterial genera was an important factor affecting the distribution of ARGs (Zhu et al., 2018; Wang et al., 2020). In Fig. 6c, the relationship between ARGs and bacteria was quite complicated in the air samples.
Ecological life strategies of microbes in response to antibiotics as a driving factor in soils
2023, Science of the Total EnvironmentOccurrence and distribution of antimicrobial resistance genes in the soil of an industrial park in China: A metagenomics survey
2021, Environmental PollutionCitation Excerpt :Most factories, especially pharmaceutical factories, are not capable of completely removing pharmaceuticals from their wastewater and these compounds might release to the surrounding environment and cause contamination (Gadipelly et al., 2014). Furthermore, it was revealed that ARGs tended to be enriched in the soil around certain pharmaceutical factory (Zhu et al., 2018). Holding numerus factories with different industrial types, the emission of ARGs in industrial parks would be more complex.
- ☆
This manuscript has been thoroughly edited by a native English speaker from an editing company (Editage by CACTUS). Editing Certificate will be provided upon request.