Changes in bacterial community structure and antibiotic resistance genes in soil in the vicinity of a pharmaceutical factory

https://doi.org/10.1016/j.ecoenv.2018.04.016Get rights and content

Highlights

  • Microbial community structure was affected by nutrients more than antibiotics.

  • Antibiotic resistance genes were enriched in the vicinity of the factory.

  • Resistance genes could be the consequence of previous antibiotic contaminations.

  • Horizontal gene transfer played an important role in spread of resistance genes.

Abstract

China is the largest global producer of antibiotics. With the demand for antibiotics increasing every year, it is necessary to assess potential environmental risks and the spread of antibiotic resistance genes (ARGs) associated with antibiotic production. Here, we investigated the occurrence and distribution of ARGs in soil in the vicinity of a pharmaceutical factory. The results showed that antibiotic concentrations were under the detection limit; however, ARGs were present in soil and tended to be enriched near the factory. A significant correlation between the relative abundance of intI-1 and tetracycline ARGs implied that horizontal gene transfer might play an important role in the spread of ARGs. The occurrence of these ARGs could be the results of previous antibiotic contamination. However, the soil bacterial community structure seemed to be more affected by nutrients or other factors than by antibiotics. Overall, this study supports the viewpoint that long-term pharmaceutical activity might have a negative effect on environmental health, thus, underscoring the need to regulate antibiotic production and management.

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).

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    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.

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