Effect of antibiotic stress on antibiotic resistance genes in soils with different fertilization histories

doi:10.3969/j.issn.1004-1524.20250024

Acta Agriculturae Zhejiangensis ›› 2026, Vol. 38 ›› Issue (3): 551-558.DOI: 10.3969/j.issn.1004-1524.20250024

• Environmental Science • Previous Articles Next Articles

Effect of antibiotic stress on antibiotic resistance genes in soils with different fertilization histories

ZHU Sengen¹(), CHENG Jianhua²^,^*(), ZHU Xingna³, LI Jianxin⁴, TANG Xiangyu²

^1. Zhejiang Honggaitou Agricultural Science and Technology Co., Ltd., Jiangshan 324109, Zhejiang, China
^2. School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China
^3. School of Modern Agriculture, Jiaxing Vocational & Technical College, Jiaxing 314036, Zhejiang, China
^4. Forestry Bureau of Jiangshan County, Jiangshan 324100, Zhejiang, China

Received:2025-01-06 Online:2026-03-25 Published:2026-04-17

Abstract

Abstract:

The effects of antibiotic selective pressure on antibiotic resistance genes (ARGs) in agricultural soils with long term application of different manures remain poorly understood. The high-throughput quantitative polymerase chain reaction technology was adopted in the present study to analyze the effect of antibiotic dose on the number, relative abundance and composition of ARGs in farmland soils subjected to long-term application of chemical fertilizers, chicken manure, and pig manure. The results showed that a total of 109 ARGs and 24 mobile genetic elements (MGEs) were detected across all soil samples. Genes conferring resistance to aminoglycosides and multiple drugs were the two most dominant types of ARGs. Long-term manure application enhanced both the number and relative abundance of soil ARGs and altered their distribution patterns, with pig manure demonstrating a more pronounced effect. Likely, antibiotic addition also stimulated the spread of ARGs in soil, while its extent increased with antibiotic concentration and varied depending on the soil fertilization history. The response of ARGs detection frequency to antibiotic stress was more pronounced in soils with a history of chemical fertilizer application, while the relative concentration and distribution patterns of ARGs in manure-amended soils showed greater sensitivity to antibiotics. Additionally, the relative abundance of soil MGEs showed a significantly (p<0.01) positive correlation with that of ARGs irrespective of soil types. These results provided a scientific basis for the evaluation of health risk of agricultural application of livestock manure.

Key words: soil, fertilization history, antibiotic stress, antibiotic resistance genes, dose-response

CLC Number:

ZHU Sengen, CHENG Jianhua, ZHU Xingna, LI Jianxin, TANG Xiangyu. Effect of antibiotic stress on antibiotic resistance genes in soils with different fertilization histories[J]. Acta Agriculturae Zhejiangensis, 2026, 38(3): 551-558.

Figures/Tables 7

Table 1 Basic physicochemical properties and antibiotic residue content of the original soil sample

样本 Sample	pH值 pH value	有机碳含量/(mg·g^-1) Organic carbon content/(mg·g^-1)	总氮含量/(mg·g^-1) Total nitrogen content/(mg·g^-1)	抗生素残留量/(μg·kg^-1) Antibiotic residue/(μg·kg^-1)
样本 Sample	pH值 pH value	有机碳含量/(mg·g^-1) Organic carbon content/(mg·g^-1)	总氮含量/(mg·g^-1) Total nitrogen content/(mg·g^-1)	SD	SMT	SMZ	OTC	DOXC
CM	5.57	22.23	1.32	6.23	2.98	1.51	5.25	7.36
PM	6.45	24.08	1.42	10.68	19.57	3.44	28.91	16.26
NPK	4.58	13.40	1.29	0.18	—	0.28	1.38	0.14

Fig.1 The number of detected antibiotic resistance genes in soils with different antibiotic addition levels PM, CM, and NPK represent the soil of upland farmlands under long-term (more than 5 years) application of pig manure, chicken manure, and chemical fertilizers, respectively. The same as below. Bars marked without the same letters indicate significan difference at p<0.05. MLSB, Macrolide-lincosamide-streptogramin B.

Fig.2 Relative abundance of detected antibiotic resistance genes in soils with different antibiotic addition levels Bars marked without the same letters indicate significan difference at p<0.05 for the same sample.

Fig.3 Distribution pattern of antibiotic resistance genes in soil based on principal coordinate analysis

Fig.4 The number of detected mobile genetic elements in soils with different antibiotic addition levels

Fig.5 Relative abundance of detected mobile genetic elements in soils with different antibiotic addition levels

Fig.6 Correlation between the relative abundance of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in soil samples

References 19

[1]	朱永官, 陈青林, 苏建强, 等. 环境中抗生素与抗性基因组的研究[J]. 科学观察, 2017, 12(6): 60-62.
	ZHU Y G, CHEN Q L, SU J Q, et al. Study on antibiotics and resistance genome in environment[J]. Science Focus, 2017, 12(6): 60-62.
[2]	LAU C H, TIEN Y C, STEDTFELD R D, et al. Impacts of multi-year field exposure of agricultural soil to macrolide antibiotics on the abundance of antibiotic resistance genes and selected mobile genetic elements[J]. Science of the Total Environment, 2020, 727: 138520.
[3]	ZHU Y G, JOHNSON T A, SU J Q, et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(9): 3435-3440.
[4]	黄丹, 叶茂, 朱国繁, 等. 抗生素/抗性细菌/抗性基因在土壤-植物系统中迁移转化及阻控消减的研究进展[J]. 土壤, 2020, 52(5): 891-900.
	HUANG D, YE M, ZHU G F, et al. Migration and risk control of antibiotic and antibiotic resistance bacteria/genes in soil-plant system: a review[J]. Soils, 2020, 52(5): 891-900.
[5]	FORSBERG K J, REYES A, WANG B, et al. The shared antibiotic resistome of soil bacteria and human pathogens[J]. Science, 2012, 337(6098):1107-1111.
[6]	ZHANG Y J, HU H W, CHEN Q L, et al. Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes[J]. Environment International, 2019, 130: 104912.
[7]	HEUER H, SMALLA K. Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months[J]. Environmental Microbiology, 2007, 9(3): 657-666.
[8]	CHEN Q L, AN X L, LI H, et al. Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil[J]. Environment International, 2016, 92/93: 1-10.
[9]	SUN S L, LU C, LIU J, et al. Antibiotic resistance gene abundance and bacterial community structure in soils altered by ammonium and nitrate concentrations[J]. Soil Biology and Biochemistry, 2020, 149: 107965.
[10]	KYSELKOVÁ M, KOTRBOVÁ L, BHUMIBHAMON G, et al. Tetracycline resistance genes persist in soil amended with cattle feces independently from chlortetracycline selection pressure[J]. Soil Biology and Biochemistry, 2015, 81: 259-265.
[11]	XU M, STEDTFELD R D, WANG F, et al. Composting increased persistence of manure-borne antibiotic resistance genes in soils with different fertilization history[J]. Science of the Total Environment, 2019, 689: 1172-1180.
[12]	叶红玉, 徐志荣, 王浙明, 等. 浙江省畜禽养殖业废水污染特征及环境风险评估研究[J]. 环境科学与管理, 2015, 40(6): 165-169.
	YE H Y, XU Z R, WANG Z M, et al. Wastewater pollution characteristics of livestock and poultry breeding in Zhejiang Province and its environmental risk assessment[J]. Environmental Science and Management, 2015, 40(6): 165-169.
[13]	ZHANG Y J, HU H W, GOU M, et al. Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics[J]. Environmental Pollution, 2017, 231: 1621-1632.
[14]	XIE W Y, YUAN S T, XU M G, et al. Long-term effects of manure and chemical fertilizers on soil antibiotic resistome[J]. Soil Biology and Biochemistry, 2018, 122: 111-119.
[15]	HAN X M, HU H W, CHEN Q L, et al. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures[J]. Soil Biology and Biochemistry, 2018, 126: 91-102.
[16]	PENG S, FENG Y Z, WANG Y M, et al. Prevalence of antibiotic resistance genes in soils after continually applied with different manure for 30 years[J]. Journal of Hazardous Materials, 2017, 340: 16-25.
[17]	QIAN X, GU J, SUN W, et al. Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting[J]. Journal of Hazardous Materials, 2018, 344: 716-722.
[18]	ZHANG Z Y, ZHANG Q, WANG T Z, et al. Assessment of global health risk of antibiotic resistance genes[J]. Nature Communications, 2022, 13: 1553.
[19]	沈聪, 张俊华, 刘吉利, 等. 宁夏养鸡场粪污和周边土壤中抗生素及抗生素抗性基因分布特征[J]. 环境科学, 2022, 43(8): 4166-4178.
	SHEN C, ZHANG J H, LIU J L, et al. Distribution characteristics of antibiotics and antibiotic resistance genes in manure and surrounding soil of poultry farm in Ningxia[J]. Environmental Science, 2022, 43(8): 4166-4178.

Effect of antibiotic stress on antibiotic resistance genes in soils with different fertilization histories

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