The behavior of antibiotic resistance genes and their associations with bacterial community during poultry manure composting
Introduction
The intensive uses of antibiotics in livestock manure industries for growth promotion and disease prevention, conjugate with medical persecution has provoke major antibiotic pollution threat to human and animal health, and afterword enhance the insertion, transmission and deposition of antibiotic resistant bacteria (ARB) and resistance genes (ARGs) in the soil and water bodies (Qian et al., 2018, Ma et al., 2017). According to recent reports of China, more than 52% of total antibiotic utilization (162,000 t) was consumed in the Chinese livestock breeding industry (Peng et al., 2018). However, to cure the animal diseases very small concentration of the antibiotics are required, and more than 30 to 90% of the antibiotics were discharge in the manure by animal excreta (Heuer et al., 2011, Jia et al., 2017). In this regard, organic chicken manure has been proven to be a prime reservoir of ARB and ARGs (Cui et al., 2016, Zhang et al., 2016a, Zhang et al., 2016b, Zhang et al., 2016c). Zhu et al. (2017) suggested that long term application of livestock manure have been increased the relative abundance (RAs) of 10 tet genes and two sul genes in soil, where Qian et al., 2016b, Guo et al., 2018 confirmed that the deposition RAs of ARGs were up to 0.28–0.45 gene copies/16S rRNA copies and can rapidly mobile in the soil via horizontal gene transfer (HGT). Subsequently, Zhu et al., 2013, Peng et al., 2018 introduced that the application of poultry manure (PM) may enriched source of ARGs especially tetracycline (text, tetw, teta, tet33, tetz and tetb), chloramphenicol (Cata11, Cata8 and Cata16) and erythromycin (ermB, ermY, ermG and ermC) into the soil, while the RAs of another ARGs were increased by at least 1 log.
However, aerobic composting is the effective bioremediation method applied to recycle the livestock manure, where it can destroy pathogens, and the residue can be exploited as an organic fertilizer (Diehl and Lapara, 2010, Cheng et al., 2013, Jia et al., 2015). But alteration in the microbial dynamics during composting may considerably affect the RAs of ARGs (Salyers and Amábile-Cuevas, 1997, Blair et al., 2014), despite this many inconsistent results have been reported in various investigation of the influence of composting on the RA of ARGs. Sun et al., 2018, Su et al., 2015 identify the impact of biochar on the RA of ARGs by meta-sequencing, where the results showed 20–52% of a mitigation ability of the total ARGs. Qian et al., 2016a, Qian et al., 2016b reported that thermophiles condition were significantly reduced the RAs of sulfonamide (sul1 and sul2), tetracycline (tetG and tetC) and aminoglycoside intI1, whereas the percentage of chloramphenicol (ermF, ermB, and tetW) and Beta-lactam resistant genes enhanced considerably. Beside this, mobile genetic elements (MGEs) can significantly alleviate the mobility of ARGs in the environment, where they primarily supplemented in the form of transposons, integrons, and insertion sequences (Udikovic-Kolic et al., 2014, Duan et al., 2017). Some previous findings have noticed that the changes in the RAs of MGEs during organic waste composting are not uniform because many environmental factors are responsible for efficient composting (Zhang et al., 2015, Wei et al., 2016).
Many studies have proven the fates of ARB and ARGs in manure composting process and soil contamination (Li et al., 2015, Xie et al., 2016), but reciprocity between the synchronal ARGs and bacterial dynamics were not identified. Subsequently, it is well proverbial that bacterial community transmutation mainly lead to the ARGs transition in compost (Yin et al., 2017). In addition, HGT via MGEs was also proven to be intimately associated with ARGs in manure (Baker-Austin et al., 2006), compost (He et al., 2016) and natural environments (Pal et al., 2015, Johnson et al., 2016, Chen et al., 2018). However, the roles of meta-genomic analysis on microbial community transition associated with the ARGs alteration in the chicken manure compost with influence of clay is still unexplored. Moreover, many culture depended and advance molecular technology including polymerase chain reaction (PCR) and real time quantitative PCR (qPCR) have been extensively applied to quantitatively and qualitatively evaluation of the occurrence, dynamics and fate of ARGs in compost (Zhang et al., 2016a, Zhang et al., 2016b, Zhang et al., 2016c, Li et al., 2017), but most of the study restricted by the use of limited numbers of primers for specific ARGs, which render it ambitious for scientist to interpret the complete biography of microbial ARBs and ARGs in the compost. Hence, pyro-sequencing empiric metagenomic analysis give potent drive to solve the above technical trouble due to its ability for broad spectrum sequence identification and precise estimation, which has been thriving to investigate the ARGs dynamics in various environmental conditions, such as compost (Jechalke et al., 2014, Tang et al., 2015), toxic metals contaminated soil (Albrecht et al., 2010) and sewage sludge (Wang et al., 2007).
In this study, metagenomic approaches was adopted to investigate the fate of a wide spectrum of ARGs distribution during PM aerobic composting, and to compare the influence of different concentration of clay amendment on the abundance, diversity and dynamics of these ARGs compost. Clay is a low-cost porous mineral which is mainly made by montmorillonite and kaolinite and its particles percent content is about to 70%. Thus this kind of natural clay can be considered to be used as composting amendment to improve the PM composting. But none of previous study reported the role of clay to ARGs during the PM composting which is not only promote microbial activities, and porosity during the composting, but also improve water holding capacity and immobilized ionic molecules. We characterized that: (i) clay amendment can substantially influence the percentage of ARGs in PM compost; (ii) to identify the correlations among the various ARGs and bacterial community and physicochemical parameters as well as gaseous emission; and (iii) to explore the dynamics of ARGs are interact with variation in bacterial species diversity, which have been acknowledged as an essential decisive of ARG concentration. This study may render our perceptions esteem of complex reciprocity between the environmental factors, ARGs and bacterial dynamics in the manure/compost with intense anthropogenic interference.
Section snippets
Raw materials collection, processing and experiment design
Aerobic composting was performed using PM and wheat straw (WS) added as a bulking agent into in-vessel composter at Northwest Agricultural and Forestry, University, Yangling, China. The clay was applied as amendment to understand the impact on ARGs and total bacteria species dynamics. The organic waste was used for this study collected from the farmhouse of Northwest Agricultural and Forestry, University, Yangling, China, while the clay was obtained from the sediment of the local mountain (Chen
Effect of clay on antibiotic resistant genes during composting
As shown in Fig. 1, Fig. 2, in the raw feedstock, the total RAs of the identified ARGs was 4.3 × 108 copies kg−1 dry weight basis, where ARGs of tetracycline, chloramphenicol, sulfonamide, vancomycin, beta-lactam and aminoglycoside were significantly very high percentage than other ARGs. Among the all ARGs, the amendment of clay was significantly reduced the RAs of tetracycline, chloramphenicol, sulfonamide, vancomycin, beta-lactam and aminoglycoside resistant genes in the compost. During the
Conclusions
This study confirmed that amendment of lower dosage of clay (4%) had significantly reduced the abundance of ARGs in PM compost. 4% clay had potential influence on bacterial dynamics and enhanced the composting. In addition, the succession of Firmicutes and Proteobacteria during the composting was the potential driver for ARGs alteration. Bacillus and Pseudomonas species were mainly involve to the ARGs profile changes. The correlation study of T3 treatment was also confirmed that not only
Acknowledgements
The authors are grateful for the financial support from a Research Fund for International Young Scientists from National Natural Science Foundation of China (Grant No. 31750110469), China and The Introduction of talent research start-up found (No. Z101021803), College of Natural Resources and Environment, Northwest Agricultural and Forestry University, Yangling, Shaanxi Province 712100, China. We are also thankful to our all laboratory colleagues and research staff members for their
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