Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China

Nan Wu , Weiyu Zhang , Shiyu Xie , Ming Zeng , Haixue Liu , Jinghui Yang , Xinyuan Liu , Fan Yang

Front. Environ. Sci. Eng. ›› 2020, Vol. 14 ›› Issue (1) : 1

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Front. Environ. Sci. Eng. ›› 2020, Vol. 14 ›› Issue (1) : 1 DOI: 10.1007/s11783-019-1180-x
RESEARCH ARTICLE
RESEARCH ARTICLE

Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China

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Abstract

• Manure application increased the abundances of ARGs and MGEs in agricultural soils.

• Five classes of ARGs and two MGEs were prevalent in manured and unfertilized soils.

• Genera Pseudomonas and Bacteroidetes might be the dominant hosts of intI1 and ermF.

• The abundances of ARGs positively correlated with TC, TN, OM, Cu, Zn, Pb and MGEs.

Land application of manure tends to result in the dissemination of antibiotic resistance in the environment. In this study, the influence of long-term manure application on the enrichment of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in agricultural soils was investigated. All the analyzed eight ARGs (tetA, tetW, tetX, sulI, sulII, ermF, aac(6’)-Ib-cr and blaTEM) and two MGEs (intI1 and Tn916/1545) were detected in both the manured and control soils, with relative abundances ranging from 10-6 to 10-2. Compared with the control soil, the relative abundances of ARGs and MGEs in manured soils were enriched 1.0–18.1 fold and 0.6–69.1 fold, respectively. High-throughput sequencing analysis suggested that at the phylum level, the bacteria carrying intI1 and ermF might be mainly affiliated with Proteobacteria and Bacteroides, respectively. The dominant genera carrying intI1 and ermF could be Pseudomonas and Bacteroides, independent of manure application. Correlation analysis revealed that ARGs had strong links with soil physicochemical properties (TC, TN, and OM), heavy metals (Cu, Zn and Pb) and MGEs, indicating that the profile and spread of ARGs might be driven by the combined impacts of multiple factors. In contrast, soil pH and C/N exhibited no significant relationships with ARGs. Our findings provide evidence that long-term manure application could enhance the prevalence and stimulate the propagation of antibiotic resistance in agricultural soils.

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Keywords

Antibiotic resistance / Mobile genetic elements / Soil / Manure / Heavy metals

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Nan Wu, Weiyu Zhang, Shiyu Xie, Ming Zeng, Haixue Liu, Jinghui Yang, Xinyuan Liu, Fan Yang. Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Front. Environ. Sci. Eng., 2020, 14(1): 1 DOI:10.1007/s11783-019-1180-x

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References

[1]

Agersø Y, Sandvang D (2005). Class 1 integrons and tetracycline resistance genes in Alcaligenes, Arthrobacter, and Pseudomonas spp. isolated from pigsties and manured soil. Applied and Environmental Microbiology, 71(12): 7941–7947

[2]

Aminov R I, Garrigues-Jeanjean N, Mackie R I (2001). Molecular ecology of tetracycline resistance: Development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Applied and Environmental Microbiology, 67(1): 22–32

[3]

Brenciani A, Tiberi E, Bacciaglia A, Petrelli D, Varaldo P E, Giovanetti E (2011). Two distinct genetic elements are responsible for erm(TR)-mediated erythromycin resistance in tetracycline-susceptible and tetracycline-resistant strains of Streptococcus pyogenes. Antimicrobial Agents and Chemotherapy, 55(5): 2106–2112

[4]

Byrne-Bailey K G, Gaze W H, Zhang L, Kay P, Boxall A, Hawkey P M, Wellington E M (2011). Integron prevalence and diversity in manured soil. Applied and Environmental Microbiology, 77(2): 684–687

[5]

Chen J, Yu Z, Michel F C Jr, Wittum T, Morrison M (2007). Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Applied and Environmental Microbiology, 73(14): 4407–4416

[6]

Chen Q, An X, Li H, Su J, Ma Y, Zhu Y G (2016). Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environment International, 92 93: 1–10

[7]

Chung W O, Werckenthin C, Schwarz S, Roberts M C (1999). Host range of the ermF rRNA methylase gene in bacteria of human and animal origin. Journal of Antimicrobial Chemotherapy, 43(1): 5–14

[8]

Cui E, Wu Y, Zuo Y, Chen H (2016). Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresource Technology, 203: 11–17

[9]

Eitel Z, Sóki J, Urbán E, Nagy E (2013). The prevalence of antibiotic resistance genes in Bacteroides fragilis group strains isolated in different European countries. Anaerobe, 21: 43–49

[10]

Forsberg K J, Reyes A, Wang B, Selleck E M, Sommer M O, Dantas G (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337(6098): 1107–1111

[11]

Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L (2012). Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Research, 46(7): 2355–2364

[12]

Gillings M R, Gaze W H, Pruden A, Smalla K, Tiedje J M, Zhu Y G (2015). Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME Journal, 9(6): 1269–1279

[13]

Guo A, Gu J, Wang X, Zhang R, Yin Y, Sun W, Tuo X, Zhang L (2017). Effects of superabsorbent polymers on the abundances of antibiotic resistance genes, mobile genetic elements, and the bacterial community during swine manure composting. Bioresource Technology, 244(Pt 1): 658–663

[14]

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

[15]

Hardwick S A, Stokes H W, Findlay S, Taylor M, Gillings M R (2008). Quantification of class 1 integron abundance in natural environments using real-time quantitative PCR. FEMS Microbiology Letters, 278(2): 207–212

[16]

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

[17]

Hvistendahl M (2012). China takes aim at rampant antibiotic resistance. Science, 336(6083): 795

[18]

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(20): 178–185

[19]

Johnsen B O, Handal N, Meisal R, Bjørnholt J V, Gaustad P, Leegaard T M (2017). erm gene distribution among Norwegian Bacteroides isolates and evaluation of phenotypic tests to detect inducible clindamycin resistance in Bacteroides species. Anaerobe, 47: 226–232

[20]

Liu P, Jia S, He X, Zhang X, Ye L (2017). Different impacts of manure and chemical fertilizers on bacterial community structure and antibiotic resistance genes in arable soils. Chemosphere, 188: 455–464

[21]

Lu R K (2000). Analysis Methods of Soil and Agricultural Chemistry. Beijing: Chinese Agriculture and Technology Press (in Chinese)

[22]

Luo G, Rensing C, Chen H, Liu M Q, Wang M, Guo S W, Ling N, Shen Q R (2018). Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Functional Ecology, 32(4): 1103–1116

[23]

Negreanu Y, Pasternak Z, Jurkevitch E, Cytryn E (2012). Impact of treated wastewater irrigation on antibiotic resistance in agricultural soils. Environmental Science & Technology, 46(9): 4800–4808

[24]

Ng L K, Martin I, Alfa M, Mulvey M (2001). Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15(4): 209–215

[25]

Nguyen C C, Hugie C N, Kile M L, Navab-Daneshmand T (2019). Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review. Frontiers of Environmental Science & Engineering, 13(3): 46

[26]

Peng S, Feng Y, Wang Y, Guo X, Chu H, Lin X (2017). Prevalence of antibiotic resistance genes in soils after continually applied with different manure for 30 years. Journal of Hazardous Materials, 340: 16–25

[27]

Pruden A, Pei R, Storteboom H, Carlson K H (2006). Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environmental Science & Technology, 40(23): 7445–7450

[28]

Pu C, Liu H, Ding G, Sun Y, Yu X, Chen J, Ren J, Gong X (2018). Impact of direct application of biogas slurry and residue in fields: In situ analysis of antibiotic resistance genes from pig manure to fields. Journal of Hazardous Materials, 344: 441–449

[29]

Rosewarne C P, Pettigrove V, Stokes H W, Parsons Y M (2010). Class 1 integrons in benthic bacterial communities: Abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance. FEMS Microbiology Ecology, 72(1): 35–46

[30]

Sharma V K, Johnson N, Cizmas L, McDonald T J, Kim H (2016). A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere, 150: 702–714

[31]

Sharma V K, Yu X, McDonald T J, Jinadatha C, Dionysiou D D, Feng M (2019). Elimination of antibiotic resistance genes and control of horizontal transfer risk by UV-based treatment of drinking water: A mini review. Frontiers of Environmental Science & Engineering, 13(3): 37

[32]

Shi J, Yu X, Zhang M, Lu S, Wu W, Wu J, Xu J (2011). Potential risks of copper, zinc, and cadmium pollution due to pig manure application in a soil-rice system under intensive farming: a case study of Nanhu, China. Journal of Environmental Quality, 40(6): 1695–1704

[33]

Suzuki M T, Taylor L T, DeLong E F (2000). Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Applied and Environmental Microbiology, 66(11): 4605–4614

[34]

Udikovic-Kolic N, Wichmann F, Broderick N A, Handelsman J (2014). Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proceedings of the National Academy of Sciences of the United States of America, 111(42): 15202–15207

[35]

Wang F H, Qiao M, Lv Z E, Guo G X, Jia Y, Su Y H, Zhu Y G (2014). Impact of reclaimed water irrigation on antibiotic resistance in public parks, Beijing, China. Environmental Pollution, 184: 247–253

[36]

Wang M, Liu P, Xiong W, Zhou Q, Wangxiao J, Zeng Z, Sun Y (2018). Fate of potential indicator antimicrobial resistance genes (ARGs) and bacterial community diversity in simulated manure-soil microcosms. Ecotoxicology and Environmental Safety, 147: 817–823

[37]

Wu N, Qiao M, Zhang B, Cheng W D, Zhu Y G (2010). Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environmental Science & Technology, 44(18): 6933–6939

[38]

Xie W Y, Yuan S T, Xu M G, Yang X P, Shen Q R, Zhang W W, Su J Q, Zhao F J (2018). Long-term effects of manure and chemical fertilizers on soil antibiotic resistome. Soil Biology & Biochemistry, 122: 111–119

[39]

Xiong W, Sun Y, Ding X, Zhang Y, Zhong X, Liang W, Zeng Z (2015). Responses of plasmid-mediated quinolone resistance genes and bacterial taxa to (fluoro)quinolones-containing manure in arable soil. Chemosphere, 119: 473–478

[40]

Xu Y, Yu W, Ma Q, Zhou H (2015). Occurrence of (fluoro)quinolones and (fluoro)quinolone resistance in soil receiving swine manure for 11 years. Science of the Total Environment, 530 531: 191–197

[41]

Yang F, Zhang K, Zhi S, Li J, Tian X, Gu Y, Zhou J (2019). High prevalence and dissemination of b-lactamase genes in swine farms in northern China. Science of the Total Environment, 651(Pt 2): 2507–2513

[42]

Zhang A N, Li L G, Ma L, Gillings M R, Tiedje J M, Zhang T (2018a). Conserved phylogenetic distribution and limited antibiotic resistance of class 1 integrons revealed by assessing the bacterial genome and plasmid collection. Microbiome, 6(1): 130

[43]

Zhang J, Chen M, Sui Q, Tong J, Jiang C, Lu X, Zhang Y, Wei Y (2016). Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting. Water Research, 91: 339–349

[44]

Zhang L, Gu J, Wang X, Zhang R, Tuo X, Guo A, Qiu L (2018b). Fate of antibiotic resistance genes and mobile genetic elements during anaerobic co-digestion of Chinese medicinal herbal residues and swine manure. Bioresource Technology, 250: 799–805

[45]

Zhang S, Zhang F, Liu X, Wang Y, Zou S, He X (2005). Determination and analysis on main harmful composition in excrement of scale livestock and poultry feedlots. Plant Nutrition and Fertilizing Science, 11(6): 822–829 (in Chinese)

[46]

Zhang X, Wu B, Zhang Y, Zhang T, Yang L, Fang H H P, Ford T, Cheng S (2009). Class 1 integronase gene and tetracycline resistance genes tetA and tetC in different water environments of Jiangsu Province, China. Ecotoxicology (London, England), 18(6): 652–660

[47]

Zhang Y J, Hu H W, Gou M, Wang J T, Chen D, He J Z (2017). Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environmental Pollution, 231(Pt 2): 1621–1632

[48]

Zhao Z, Wang J, Han Y, Chen J, Liu G, Lu H, Yan B, Chen S (2017). Nutrients, heavy metals and microbial communities co-driven distribution of antibiotic resistance genes in adjacent environment of mariculture. Environmental Pollution, 220(Pt B): 909–918

[49]

Zhou X, Qiao M, Wang F H, Zhu Y G (2017). Use of commercial organic fertilizer increases the abundance of antibiotic resistance genes and antibiotics in soil. Environmental Science and Pollution Research International, 24(1): 701–710

[50]

Zhu B, Chen Q, Chen S, Zhu Y G (2017). Does organically produced lettuce harbor higher abundance of antibiotic resistance genes than conventionally produced? Environment International, 98: 152–159

[51]

Zhu Y G, Johnson T A, Su J Q, Qiao M, Guo G X, Stedtfeld R D, Hashsham S A, Tiedje J M (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110(9): 3435–3440

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