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

Yuwei Guo , Xian Xiao , Yuan Zhao , Jianguo Liu , Jizhong Zhou , Bo Sun , Yuting Liang

Front. Environ. Sci. Eng. ›› 2022, Vol. 16 ›› Issue (7) : 91

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Front. Environ. Sci. Eng. ›› 2022, Vol. 16 ›› Issue (7) : 91 DOI: 10.1007/s11783-021-1499-y
RESEARCH ARTICLE
RESEARCH ARTICLE

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

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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.

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Keywords

Pig manure / Antibiotics / Metals / Antibiotic resistance genes / Paddy fields

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Yuwei Guo, Xian Xiao, Yuan Zhao, Jianguo Liu, Jizhong Zhou, Bo Sun, Yuting Liang. Antibiotic resistance genes in manure-amended paddy soils across eastern China: Occurrence and influencing factors. Front. Environ. Sci. Eng., 2022, 16(7): 91 DOI:10.1007/s11783-021-1499-y

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References

[1]

An J, Chen H, Wei S, Gu J (2015). Antibiotic contamination in animal manure, soil, and sewage sludge in Shenyang, Northeast China. Environmental Earth Sciences, 74(6): 5077–5086

[2]

Baker-Austin C, Wright M S, Stepanauskas R, McArthur J V (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4): 176–182

[3]

Berg J, Tom-Petersen A, Nybroe O (2005). Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Letters in Applied Microbiology, 40(2): 146–151

[4]

Chopra I, Roberts M (2001). Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews, 65(2): 232–260

[5]

Cui E P, Gao F, Liu Y, Fan X Y, Li Z Y, Du Z J, Hu C, Neal A L (2018). Amendment soil with biochar to control antibiotic resistance genes under unconventional water resources irrigation: Proceed with caution. Environmental Pollution, 240: 475–484

[6]

Deng W, Zhang A, Chen S, He X, Jin L, Yu X, Yang S, Li B, Fan L, Ji L, Pan X, Zou L (2020). Heavy metals, antibiotics and nutrients affect the bacterial community and resistance genes in chicken manure composting and fertilized soil. Journal of Environmental Management, 257: 109980

[7]

González-Alcaraz M N, van Gestel C A M (2015). Climate change effects on enchytraeid performance in metal-polluted soils explained from changes in metal bioavailability and bioaccumulation. Environmental Research, 142: 177–184

[8]

Guo T, Lou C, Zhai W, Tang X, Hashmi M Z, Murtaza R, Li Y, Liu X, Xu J (2018). Increased occurrence of heavy metals, antibiotics and resistance genes in surface soil after long-term application of manure. Science of the Total Environment, 635: 995–1003

[9]

Heuer H, Schmitt H, Smalla K (2011a). Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology, 14(3): 236–243

[10]

Heuer H, Solehati Q, Zimmerling U, Kleineidam K, Schloter M, Müller T, Focks A, Thiele-Bruhn S, Smalla K (2011b). Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Applied and Environmental Microbiology, 77(7): 2527–2530

[11]

Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012). Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. Journal of Hazardous Materials, 235–236: 178–185

[12]

Johnsen P J, Townsend J P, Bøhn T, Simonsen G S, Sundsfjord A, Nielsen K M (2009). Factors affecting the reversal of antimicrobial-drug resistance. Lancet. Infectious Diseases, 9(6): 357–364

[13]

Kemper N (2008). Veterinary antibiotics in the aquatic and terrestrial environment. Ecological Indicators, 8(1): 1–13

[14]

Kim S Y, Kuppusamy S, Kim J H, Yoon Y E, Kim K R, Lee Y B (2016). Occurrence and diversity of tetracycline resistance genes in the agricultural soils of Korea. Environmental Science and Pollution Research International, 23(21): 22190–22196

[15]

Knapp C W, McCluskey S M, Singh B K, Campbell C D, Hudson G, Graham D W (2011). Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One, 6(11): e27300

[16]

Kolz A C, Moorman T B, Ong S K, Scoggin K D, Douglass E A (2005). Degradation and metabolite production of tylosin in anaerobic and aerobic swine-manure lagoons. Water Environment Research, 77(1): 49–56

[17]

Li Y X, Zhang X L, Li W, Lu X F, Liu B, Wang J (2013). The residues and environmental risks of multiple veterinary antibiotics in animal faeces. Environmental Monitoring and Assessment, 185(3): 2211–2220

[18]

Liang Y, Pei M, Wang D, Cao S, Xiao X, Sun B (2017). Improvement of soil ecosystem multifunctionality by dissipating Manure-Induced antibiotics and resistance genes. Environmental Science & Technology, 51(9): 4988–4998

[19]

Liu W, Zeng D, She L, Su W, He D, Wu G, Ma X, Jiang S, Jiang C, Ying G (2020). Comparisons of pollution characteristics, emission situations, and mass loads for heavy metals in the manures of different livestock and poultry in China. Science of the Total Environment, 734: 139023

[20]

Lu R (1999). Soil Agricultural Chemical Analysis. Nanjing: China Agricultural Science and Technology Press (in Chinese)

[21]

Luo L, Ma Y, Zhang S, Wei D, Zhu Y G (2009). An inventory of trace element inputs to agricultural soils in China. Journal of Environmental Management, 90(8): 2524–2530

[22]

Mahmoud M A M, Abdel-Mohsein H S (2019). Hysterical tetracycline in intensive poultry farms accountable for substantial gene resistance, health and ecological risk in Egypt- manure and fish. Environmental Pollution, 255(Pt 1): 113039

[23]

Martínez-Carballo E, González-Barreiro C, Scharf S, Gans O (2007). Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environmental Pollution, 148(2): 570–579

[24]

Pan X, Qiang Z, Ben W, Chen M (2011). Residual veterinary antibiotics in swine manure from concentrated animal feeding operations in Shandong Province, China. Chemosphere, 84(5): 695–700

[25]

Pan M, Chu L M (2016). Adsorption and degradation of five selected antibiotics in agricultural soil. Science of the Total Environment, 545–546: 48–56

[26]

Pei R, Cha J, Carlson K H, Pruden A (2007). Response of antibiotic resistance genes (ARG) to biological treatment in dairy lagoon water. Environmental Science & Technology, 41(14): 5108–5113

[27]

Rahman M M, Shan J, Yang P, Shang X, Xia Y, Yan X (2018). Effects of long-term pig manure application on antibiotics, abundance of antibiotic resistance genes (ARGs), anammox and denitrification rates in paddy soils. Environmental Pollution, 240: 368–377

[28]

Tang X, Lou C, Wang S, Lu Y, Liu M, Hashmi M Z, Liang X, Li Z, Liao Y, Qin W, Fan F, Xu J, Brookes P C (2015). Effects of long-term manure applications on the occurrence of antibiotics and antibiotic resistance genes (ARGs) in paddy soils: Evidence from four field experiments in south of China. Soil Biology and Biochemistry, 90: 179–187

[29]

Van den Meersche T, Rasschaert G, Haesebrouck F, Van Coillie E, Herman L, Van Weyenberg S, Daeseleire E, Heyndrickx M (2019). Presence and fate of antibiotic residues, antibiotic resistance genes and zoonotic bacteria during biological swine manure treatment. Ecotoxicology and Environmental Safety, 175: 29–38

[30]

Van den Meersche T, Rasschaert G, Vanden Nest T, Haesebrouck F, Herman L, Van Coillie E, Van Weyenberg S, Daeseleire E, Heyndrickx M (2020). Longitudinal screening of antibiotic residues, antibiotic resistance genes and zoonotic bacteria in soils fertilized with pig manure. Environmental Science and Pollution Research International, 27(22): 28016–28029

[31]

Wang L, Wang J, Wang J, Zhu L, Conkle J L, Yang R (2020). Soil types influence the characteristic of antibiotic resistance genes in greenhouse soil with long-term manure application. Journal of Hazardous Materials, 392: 122334

[32]

Wang L, Zhao X, Wang J, Wang J, Zhu L, Ge W (2019). Macrolide- and quinolone-resistant bacteria and resistance genes as indicators of antibiotic resistance gene contamination in farmland soil with manure application. Ecological Indicators, 106: 105456

[33]

Yang S, Qu Y, Ma J, Liu L, Wu H, Liu Q, Gong Y, Chen Y, Wu Y (2020). Comparison of the concentrations, sources, and distributions of heavy metal(loid)s in agricultural soils of two provinces in the Yangtze River Delta, China. Environmental Pollution, 264: 114688

[34]

Zhang Q Q, Tian G M, Jin R C (2018). The occurrence, maintenance, and proliferation of antibiotic resistance genes (ARGs) in the environment: influencing factors, mechanisms, and elimination strategies. Applied Microbiology and Biotechnology, 102(19): 8261–8274

[35]

Zhang R, Tang J, Li J, Zheng Q, Liu D, Chen Y, Zou Y, Chen X, Luo C, Zhang G (2013). Antibiotics in the offshore waters of the Bohai Sea and the Yellow Sea in China: Occurrence, distribution and ecological risks. Environmental Pollution, 174: 71–77

[36]

Zhou B, Wang C, Zhao Q, Wang Y, Huo M, Wang J, Wang S (2016). Prevalence and dissemination of antibiotic resistance genes and coselection of heavy metals in Chinese dairy farms. Journal of Hazardous Materials, 320: 10–17

[37]

Zhou J, Bruns M A, Tiedje J M (1996). DNA recovery from soils of diverse composition. Applied and Environmental Microbiology, 62(2): 316–322

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