Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors

doi:10.1007/s11783-021-1499-y

Front. Environ. Sci. Eng.

2022, Vol. 16

Issue (7) : 91 https://doi.org/10.1007/s11783-021-1499-y

RESEARCH ARTICLE

Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors

Yuwei Guo^1,², Xian Xiao¹, Yuan Zhao¹, Jianguo Liu¹, Jizhong Zhou^3,^4,⁵, Bo Sun², Yuting Liang²(

)

¹. School of Environmental and Safety Engineering, Changzhou University, Changzhou 213164, China
². State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China
³. Institute for Environmental Genomics, Department of Microbiology and Plant Biology, and School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019, USA
⁴. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China
⁵. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA 94270, USA

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Abstract

• Manure fertilization resulted in antibiotic residues and increased metal contents.

• The tet and sul genes were significantly enhanced with manure fertilization.

• Soil physicochemical properties contributed to 12% of the variations in ARGs.

• Soil metals and antibiotics co-select for ARGs.

Pig manure, rich in antibiotics and metals, is widely applied in paddy fields as a soil conditioner, triggering the proliferation of antibiotic resistance genes (ARGs) in soil. However, comprehensive studies on the effects of manure fertilization on the abundance of ARGs and their influencing factors are still insufficient. Here, pig manure and manure-amended and inorganic-amended soils were collected from 11 rice-cropping regions in eastern China, and the accumulation of antibiotics, metals, and ARGs was assessed simultaneously. The results showed that manure fertilization led to antibiotic residues and increased the metal content (i.e., Zn, Cu, Ni, and Cr). Tetracycline and sulfonamide resistance genes (tetM, tetO, sul1, and sul2) were also significantly enhanced with manure fertilization. According to variance partitioning analysis, the most important factors that individually influenced ARGs were soil physicochemical properties, accounting for 12% of the variation. Significant correlations between soil nutrients and ARGs indicated that manure application enhanced the growth of resistant microorganisms by supplying more nutrients. Metals and antibiotics contributed 9% and 5% to the variations in ARGs, respectively. Their co-occurrence also increased the enrichment of ARGs, as their interactions accounted for 2% of the variation in ARGs. Interestingly, Cu was significantly related to most ARGs in the soil (r = 0.26–0.52, p<0.05). Sulfapyridine was significantly related to sul2, and tetracycline resistance genes were positively related to doxycycline. This study highlighted the risks of antibiotic and ARG accumulation with manure fertilization and shed light on the essential influencing factors of ARGs in paddy soils.

Keywords Pig manure Antibiotics Metals Antibiotic resistance genes Paddy fields

Corresponding Author(s): Yuting Liang

Issue Date: 23 November 2021

Cite this article:

Yuwei Guo,Xian Xiao,Yuan Zhao, et al. Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors[J]. Front. Environ. Sci. Eng., 2022, 16(7): 91.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-021-1499-y
https://academic.hep.com.cn/fese/EN/Y2022/V16/I7/91

Tab.1 Soil physicochemical properties in inorganic-amended and manure-amended paddy soils

Fig.1 (a) Antibiotic concentrations in manure-amended paddy soils and pig manure used as fertilizer in 11 rice planting regions in eastern China; (b) Correlating the antibiotics in manure-amended paddy soils with those in pig manure. Four classes of antibiotics include tetracyclines (TCs: tetracycline; chlortetracycline; oxytetracycline; doxycycline), sulfonamides (SAs: sulfamethyldiazine; sulfamethazine; sulfadiazine; sulfapyridine; sulfamethoxazole), quinolones (FQs: norfloxacin; enrofloxacin; ciprofloxacin; lomefloxacin), and macrolides (MALs: tylosin; roxithromycin). TZ: Taizhou; MG: Mingguang; DY: Danyang; CZ: Changzhou; LA: Lu’an; SH: Shanghai; JX: Jiaxing; YW: Yiwu; SG: Shanggao; ZS: Zhangshu; FZ: Fuzhou. The left y-axis of Fig. 1 (a) represents antibiotic concentrations in manure-amended paddy soils, and the right y-axis represents antibiotic concentrations in pig manure. raw_r² and cv_r² indicate the r² value of linear regression with and without cross-validation, respectively. * and ** above the bars indicate significant differences in antibiotic concentrations between pig manure and manure-amended paddy soils at p<0.05 and p<0.01, respectively.

Fig.2 (a) Metals in inorganic-amended and manure-amended paddy soils and pig manure used as fertilizer in 11 rice planting regions in eastern China; (b) Comparison of the metals in inorganic-amended and manure-amended paddy soils. TZ: Taizhou; MG: Mingguang; DY: Danyang; CZ: Changzhou; LA: Lu’an; SH: Shanghai; JX: Jiaxing; YW: Yiwu; SG: Shanggao; ZS: Zhangshu; FZ: Fuzhou. Different letters above the bars indicate differences in metal concentrations between inorganic-amended and manure-amended paddy soils and pig manure at p<0.05. * and *** indicate significant differences in metals in inorganic-amended and manure-amended paddy soils at p<0.05 and p<0.001, respectively. n.s.: not significant.

Fig.3 (a) The relative abundance of antibiotic resistance genes in inorganic-amended and manure-amended paddy soils in 11 rice planting regions in eastern China; (b) Comparison of the relative abundance of antibiotic resistance genes in inorganic-amended and manure-amended paddy soils. tet, sul, qnr, and ermF indicate tetracycline, sulfonamide, quinolone, and macrolide resistance genes, respectively. TZ: Taizhou; MG: Mingguang; DY: Danyang; CZ: Changzhou; LA: Lu’an; SH: Shanghai; JX: Jiaxing; YW: Yiwu; SG: Shanggao; ZS: Zhangshu; FZ: Fuzhou. Different letters above the bars indicate the difference in the sum relative abundance of antibiotic resistance genes between inorganic-amended and manure-amended paddy soils at p<0.05. ** and *** indicate significant differences in antibiotic resistance genes in inorganic-amended and manure-amended paddy soils at p<0.01 and p<0.001, respectively. n.s.: not significant.

Fig.4 Pearson’s correlations between the antibiotic resistance genes and the antibiotics, metals, and other environmental variables in manure-amended paddy soils. The color points indicate a significant correlation coefficient (p<0.05; bluer indicates a stronger negative correlation, and redder indicates a stronger positive correlation). TCs: tetracyclines; SAs: sulfonamides; FQs: quinolones; MALs: macrolides; MAT: mean annual temperature; TOC: total organic carbon; TN: total nitrogen; TON: total organic nitrogen; TP: total phosphorus; AP: available phosphorus; TK: total potassium.

Fig.5 Variation partitioning analysis of the antibiotic resistance genes explained by antibiotics, metals, climatic factors, and soil properties. Metals included Zn, Cu, Pb, Ni, Cr, and Cd. Antibiotics included tetracyclines, sulfonamides, quinolones, and macrolides. Climatic factors included mean annual temperature and precipitation. Soil properties included soil moisture, SO₄²^–, total organic carbon, total nitrogen, NO₃^–-N, total organic nitrogen, total phosphorus, and available phosphorus.

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