鸡粪与中药渣共堆肥对抗生素抗性基因的影响
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摘要
畜禽粪便是抗生素抗性基因(antibiotic resistant genes,ARGs)进入环境的重要途径,为了削减畜禽粪便中的ARGs,在为期46 d的鸡粪与中药渣共堆肥后,对不同阶段ARGs和可移动基因元件(mobile gene elements,MGEs)的丰度通过实时定量PCR进行检测. 100种ARGs中检测到21种,以及2种整合酶基因(int I1和int I2)和3种转座酶基因(tnp A-01、tnp A-02和tnp A-03).结果表明,在堆肥过程中5种MGEs均显著降低,其中tnp A-01和tnp A-02去除效果最好,减少了两个数量级;氨基糖苷类抗性基因aac A/aph D和aad E显著性降低(P <0. 05);β-内酰胺类抗性基因bla OXA1与堆肥天数显著相关(P=0. 016),其去除率为78. 63%;林可酰胺类抗性基因均随堆肥时间显著降低,平均去除率为90. 39%;四环素类抗性基因的去除效果相差较大,tet G降低了99. 77%,tetR仅降低了31. 72%;喹诺酮类抗性基因qnr D去除率最高为99. 89%;磺胺类中sulⅢ的去除率高达99. 88%,而sulⅠ呈增长趋势. ARGs与MGEs相关性表明tnp A-01与ARGs之间具有显著相关性(P <0. 05). ARGs随堆肥时间的变化趋势表明,中药渣与鸡粪共堆肥可显著降低ARGs丰度,从而降低畜禽粪便在农田施用中ARGs扩散的风险.
Livestock manure is an important pathway by which antibiotic resistance genes( ARGs) enter the environment. To reduce the occurrence of antibiotic resistance genes in manures,we studied the variations of ARGs and mobile gene elements( MGEs) during the 46-day co-composting of chicken manure with Chinese medicinal herbal residues. The abundance of 100 ARGs and 5 MGEs were measured by Real-Time Quantitative PCR with 0,3,7,14,28,and 46 d co-composting. We detected 21 ARGs,2 integrase genes( int I1 and int I2),and 3 transposase genes( tnp A-01,tnp A-02,and tnp A-03). The abundance of 5 MGEs significantly declined with co-composting time,particularly tnp A-01 and tnp A-02,which were reduced by two orders of magnitude. The abundance of aac A/aph D and aad E were significantly reduced( P < 0. 05) in aminoglycoside resistance genes. In β-lactam resistance genes,the strongest relationships were demonstrated between bla OXA1 and compost days( P = 0. 016),and the removal rate was 78. 63%. The average removal rate was 90. 39% for amide resistance genes,which decreased significantly with composting time. The removal ratios were different among tetracycline resistance genes. For example,the removal ratios of tet G and tetR were 99. 77% and 31. 72%,respectively. The highest removal rate of qnr D was 99. 89%. The removal rate of sulⅢ was as high as 99. 88%,while sulⅠ showed an increasing trend. Correlations between ARGs and MGEs were significant correlation for tnp A-01 and ARGs( P < 0. 05). The trend of ARGs with composting time indicates that the composting of Chinese medicine residues and chicken manure can significantly reduce the abundance of ARGs,thus reducing the risk of ARGs being distributed via livestock manure application.
Livestock manure is an important pathway by which antibiotic resistance genes( ARGs) enter the environment. To reduce the occurrence of antibiotic resistance genes in manures,we studied the variations of ARGs and mobile gene elements( MGEs) during the 46-day co-composting of chicken manure with Chinese medicinal herbal residues. The abundance of 100 ARGs and 5 MGEs were measured by Real-Time Quantitative PCR with 0,3,7,14,28,and 46 d co-composting. We detected 21 ARGs,2 integrase genes( int I1 and int I2),and 3 transposase genes( tnp A-01,tnp A-02,and tnp A-03). The abundance of 5 MGEs significantly declined with co-composting time,particularly tnp A-01 and tnp A-02,which were reduced by two orders of magnitude. The abundance of aac A/aph D and aad E were significantly reduced( P < 0. 05) in aminoglycoside resistance genes. In β-lactam resistance genes,the strongest relationships were demonstrated between bla OXA1 and compost days( P = 0. 016),and the removal rate was 78. 63%. The average removal rate was 90. 39% for amide resistance genes,which decreased significantly with composting time. The removal ratios were different among tetracycline resistance genes. For example,the removal ratios of tet G and tetR were 99. 77% and 31. 72%,respectively. The highest removal rate of qnr D was 99. 89%. The removal rate of sulⅢ was as high as 99. 88%,while sulⅠ showed an increasing trend. Correlations between ARGs and MGEs were significant correlation for tnp A-01 and ARGs( P < 0. 05). The trend of ARGs with composting time indicates that the composting of Chinese medicine residues and chicken manure can significantly reduce the abundance of ARGs,thus reducing the risk of ARGs being distributed via livestock manure application.
引文
[1] Pruden A,Pei R T,Storteboom H,et al. Antibiotic resistance genes as emerging contaminants:studies in northern Colorado[J]. Environmental Science&Technology,2006,40(23):7445-7450.
[2] Knapp C W,Engemann C A,Hanson M L,et al. Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures[J]. Environmental Science&Technology,2008,42(14):5348-5353.
[3] Ash R J,Mauck B,Morgan M. Antibiotic resistance of gramnegative bacteria in rivers, United States[J]. Emerging Infectious Diseases,2002,8(7):713-716.
[4] Gogarten J P,Townsend J P. Horizontal gene transfer,genome innovation and evolution[J]. Nature Reviews Microbiology,2005,3(9):679-687.
[5] Fouace J. Transfer of resistance plasmids in staphylococcus aureus[J]. Annales de Microbiologie,1974,125(4):517-520.
[6]罗义,周启星.抗生素抗性基因(ARGs)———一种新型环境污染物[J].环境科学学报,2008,28(8):1499-1505.Luo Y,Zhou Q X. Antibiotic resistance genes(ARGs)as emerging pollutants[J]. Acta Scientiae Circumstantiae,2008,28(8):1499-1505.
[7] Marti R,Scott A,Tien Y C,et al. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest[J]. Applied and Environmental Microbiology,2013,79(18):5701-5709.
[8] Udikovic-Kolic N,Wichmann F,Broderick N A,et al. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization[J]. Proceedings of the National Academy of Sciences of the United States of America,2014,111(42):15202-15207.
[9] Seyfried E E,Newton R J,Rubert K F,et al. Occurrence of tetracycline resistance genes in aquaculture facilities with varying use of oxytetracycline[J]. Microbial Ecology,2010,59(4):799-807.
[10]周启星,罗义,王美娥.抗生素的环境残留、生态毒性及抗性基因污染[J].生态毒理学报,2007,2(3):243-251.Zhou Q X,Luo Y,Wang M E. Environmental residues and ecotoxicity of antibiotics and their resistance gene pollution:a review[J]. Asian Journal of Ecotoxicology,2007,2(3):243-251.
[11]邹威,罗义,周启星.畜禽粪便中抗生素抗性基因(ARGs)污染问题及环境调控[J].农业环境科学学报,2014,33(12):2281-2287.Zou W, Luo Y, Zhou Q X. Pollution and environmental regulation of antibiotic resistance genes(ARGs)in livestock manure[J]. Journal of Agro-Environment Science,2014,33(12):2281-2287.
[12] Cui E P,Wu Y,Zuo Y R,et al. Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting[J]. Bioresource Technology,2016,203:11-17.
[13]王晓慧.禽畜粪便堆肥过程中耐药基因变化的研究[D].上海:华东师范大学,2017. 8-12.Wang X H. Study on the change of ARGs in composting of livestock and poultry manure[D]. Shanghai:East China Normal University,2017. 8-12.
[14]郑宁国,黄南,王卫卫,等.高温堆肥过程对猪粪来源抗生素抗性基因的影响[J].环境科学,2016,37(5):1986-1992.Zheng N G,Huang N,Wang W W,et al. Effects of thermophilic composting on antibiotic resistance genes(ARGs)of swine manure source[J]. Environmental Science,2016,37(5):1986-1992.
[15]杨冰,丁斐,李伟东,等.中药渣综合利用研究进展及生态化综合利用模式[J].中草药,2017,48(2):377-383.Yang B, Ding F, Li W D, et al. Research progress on comprehensive utilization of Chinese medicine residue and ecological comprehensive utilization pattern[J]. Chinese Traditional and Herbal Drugs,2017,48(2):377-383.
[16]王引权,吴小琴,朱田田,等.中药固渣堆肥利用研究[J].中药材,2008,31(11):1622-1624.Wang Y Q,Wu X Q,Zhu T T,et al. Study on utilization of solid slag compost of Chinese medicinal herbal[J]. Journal of Chinese Medicinal Materials,2008,31(11):1622-1624.
[17]张红刚,滕婧,李顺祥,等.资源节约-中药渣高效综合利用研究进展[J].广州化工,2013,41(12):16-18.Zhang H G, Teng J, Li S X, et al. Research progress of comprehensive utilization of Chinese medicine residue for resources conservation[J]. Guangzhou Chemical Industry,2013,41(12):16-18.
[18]肖瑛琼,叶发兵.中药渣生物有机肥的制备及检测[J].湖北师范大学学报:自然科学版,2017,37(3):37-42.Xiao Y Q,Ye F B. Preparation and analysis of biological organic fertilizer with the reside of Chinese medicine[J]. Journal of Hubei Normal University(Natural Science),2017,37(3):37-42.
[19]王引权,Schuchardt F,陈晖,等.翻堆频率对中药渣堆肥过程及其理化性质的影响[J].中国农学通报,2012,28(29):247-252.Wang Y Q,Schuchardt F,Chen H,et al. Effects of turning frequency on chemical and physical properties in windrow composting of spent Chinese herbal medicine[J]. Chinese Agricultural Science Bulletin,2012,28(29):247-252.
[20] 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.
[21]宿程远,郑鹏,阮祁华,等.中药渣与城市污泥好氧共堆肥的效能[J].环境科学,2016,37(10):4062-4068.Su C Y,Zhen P,Ruan Q H,et al. Efficiency of aerobic cocomposting of urban sludge and Chinese medicinal herbal residues[J]. Environmental Science,2016,37(10):4062-4068.
[22] Qian X,Sun W,Gu J,et al. Reducing antibiotic resistance genes,integrons,and pathogens in dairy manure by continuous thermophilic composting[J]. Bioresource Technology,2016,220:425-432.
[23] Ghosh S,Ramsden S J,La Para T M. The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants[J]. Applied Microbiology and Biotechnology,2009,84(4):791-796.
[24] Ma Y J,Wilson C A,Novak J T,et al. Effect of various sludge digestion conditions on sulfonamide,macrolide,and tetracycline resistance genes and class I integrons[J]. Environmental Science&Technology,2011,45(18):7855-7861.
[25] Zhang J Y,Chen M X,Sui Q W,et al. Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting[J]. Water Research,2016,91:339-349.
[26] Zhang L,Gu J,Wang X J, et al. Behavior of antibiotic resistance genes during co-composting of swine manure with Chinese medicinal herbal residues[J]. Bioresource Technology,2017,244:252-260.
[27] Wright G D. The antibiotic resistome:the nexus of chemical and genetic diversity[J]. Nature Reviews Microbiology,2007,5(3):175-186.
[28] Yang B,Meng L,Xue N D. Removal of five fluoroquinolone antibiotics during broiler manure composting[J]. Environmental Technology,2018,39(3):373-381.
[29] Selvam A,Xu D L,Zhao Z Y,et al. Fate of tetracycline,sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure[J].Bioresource Technology,2012,126:383-390.
[30] Li J J, Xin Z H, Zhang Y Z, et al. Long-term manure application increased the levels of antibiotics and antibiotic resistance genes in a greenhouse soil[J]. Applied Soil Ecology,2017,121:193-200.
[31]崔二苹.生物质炭对粪肥堆肥过程中抗生素抗性基因行为特征的影响[D].杭州:浙江大学,2016. 38-43.Cui E P. The effect of biochar addition on antibiotic resistance genes during manure composting[D]. Hangzhou:Zhejiang University,2016. 38-43.
[32] Erickson M C,Liao J,Boyhan G,et al. Fate of manure-borne pathogen surrogates in static composting piles of chicken litter and peanut hulls[J]. Bioresource Technology,2010,101(3):1014-1020.
[33] Fang H,Wang H F,Cai L,et al. Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey[J].Environmental Science&Technology,2015,49(2):1095-1104.
[34] Skld O. Sulfonamide resistance:mechanisms and trends[J].Drug Resistance Updates,2000,3(3):155-160.
[35] Partridge S R,Tsafnat G,Coiera E,et al. Gene cassettes and cassette arrays in mobile resistance integrons[J]. FEMS Microbiology Reviews,2009,33(4):757-784.
[36] Hu H W,Wang J T,Li J,et al. Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils[J]. Environmental Microbiology,2016,18(11):3896-3909.
[37] Han X M,Hu H W,Shi X Z,et al. Impacts of reclaimed water irrigation on soil antibiotic resistome in urban parks of Victoria,Australia.[J]. Environmental Pollution,2016,211:48-57.
[38] Wang F H,Qiao M,Chen Z,et al. Antibiotic resistance genes in manure-amended soil and vegetables at harvest[J].Journal of Hazardous Materials,2015,299:215-221.
[39] 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.
[40] Rosser S J,Young H K. Identification and characterization of class 1 integrons in bacteria from an aquatic environment[J].Journal of Antimicrobial Chemotherapy,1999,44(1):11-18.
[41] Wang F H,Qiao M,Lv Z E,et al. Impact of reclaimed water irrigation on antibiotic resistance in public parks,Beijing,China[J]. Environmental Pollution,2014,184:247-253.
[42] Gillings M R,Krishnan S,Worden P J,et al. Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples[J]. FEMS Microbiology Letters,2008,287(1):56-62.
[43] He L Y,Liu Y S,Su H C,et al. Dissemination of antibiotic resistance genes in representative broiler feedlots environments:Identification of indicator ARGs and correlations with environmental variables[J]. Environmental Science&Technology,2014,48(22):13120-13129.
[44] Li X L,Shi L,Yang W Q,et al. New array of aacA4-catB3-dfrA1 gene cassettes and a noncoding cassette from a class-1-integron-positive clinical strain of Pseudomonas aeruginosa[J].Antimicrobial Agents and Chemotherapy,2006,50(6):2278-2279.
[2] Knapp C W,Engemann C A,Hanson M L,et al. Indirect evidence of transposon-mediated selection of antibiotic resistance genes in aquatic systems at low-level oxytetracycline exposures[J]. Environmental Science&Technology,2008,42(14):5348-5353.
[3] Ash R J,Mauck B,Morgan M. Antibiotic resistance of gramnegative bacteria in rivers, United States[J]. Emerging Infectious Diseases,2002,8(7):713-716.
[4] Gogarten J P,Townsend J P. Horizontal gene transfer,genome innovation and evolution[J]. Nature Reviews Microbiology,2005,3(9):679-687.
[5] Fouace J. Transfer of resistance plasmids in staphylococcus aureus[J]. Annales de Microbiologie,1974,125(4):517-520.
[6]罗义,周启星.抗生素抗性基因(ARGs)———一种新型环境污染物[J].环境科学学报,2008,28(8):1499-1505.Luo Y,Zhou Q X. Antibiotic resistance genes(ARGs)as emerging pollutants[J]. Acta Scientiae Circumstantiae,2008,28(8):1499-1505.
[7] Marti R,Scott A,Tien Y C,et al. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest[J]. Applied and Environmental Microbiology,2013,79(18):5701-5709.
[8] Udikovic-Kolic N,Wichmann F,Broderick N A,et al. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization[J]. Proceedings of the National Academy of Sciences of the United States of America,2014,111(42):15202-15207.
[9] Seyfried E E,Newton R J,Rubert K F,et al. Occurrence of tetracycline resistance genes in aquaculture facilities with varying use of oxytetracycline[J]. Microbial Ecology,2010,59(4):799-807.
[10]周启星,罗义,王美娥.抗生素的环境残留、生态毒性及抗性基因污染[J].生态毒理学报,2007,2(3):243-251.Zhou Q X,Luo Y,Wang M E. Environmental residues and ecotoxicity of antibiotics and their resistance gene pollution:a review[J]. Asian Journal of Ecotoxicology,2007,2(3):243-251.
[11]邹威,罗义,周启星.畜禽粪便中抗生素抗性基因(ARGs)污染问题及环境调控[J].农业环境科学学报,2014,33(12):2281-2287.Zou W, Luo Y, Zhou Q X. Pollution and environmental regulation of antibiotic resistance genes(ARGs)in livestock manure[J]. Journal of Agro-Environment Science,2014,33(12):2281-2287.
[12] Cui E P,Wu Y,Zuo Y R,et al. Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting[J]. Bioresource Technology,2016,203:11-17.
[13]王晓慧.禽畜粪便堆肥过程中耐药基因变化的研究[D].上海:华东师范大学,2017. 8-12.Wang X H. Study on the change of ARGs in composting of livestock and poultry manure[D]. Shanghai:East China Normal University,2017. 8-12.
[14]郑宁国,黄南,王卫卫,等.高温堆肥过程对猪粪来源抗生素抗性基因的影响[J].环境科学,2016,37(5):1986-1992.Zheng N G,Huang N,Wang W W,et al. Effects of thermophilic composting on antibiotic resistance genes(ARGs)of swine manure source[J]. Environmental Science,2016,37(5):1986-1992.
[15]杨冰,丁斐,李伟东,等.中药渣综合利用研究进展及生态化综合利用模式[J].中草药,2017,48(2):377-383.Yang B, Ding F, Li W D, et al. Research progress on comprehensive utilization of Chinese medicine residue and ecological comprehensive utilization pattern[J]. Chinese Traditional and Herbal Drugs,2017,48(2):377-383.
[16]王引权,吴小琴,朱田田,等.中药固渣堆肥利用研究[J].中药材,2008,31(11):1622-1624.Wang Y Q,Wu X Q,Zhu T T,et al. Study on utilization of solid slag compost of Chinese medicinal herbal[J]. Journal of Chinese Medicinal Materials,2008,31(11):1622-1624.
[17]张红刚,滕婧,李顺祥,等.资源节约-中药渣高效综合利用研究进展[J].广州化工,2013,41(12):16-18.Zhang H G, Teng J, Li S X, et al. Research progress of comprehensive utilization of Chinese medicine residue for resources conservation[J]. Guangzhou Chemical Industry,2013,41(12):16-18.
[18]肖瑛琼,叶发兵.中药渣生物有机肥的制备及检测[J].湖北师范大学学报:自然科学版,2017,37(3):37-42.Xiao Y Q,Ye F B. Preparation and analysis of biological organic fertilizer with the reside of Chinese medicine[J]. Journal of Hubei Normal University(Natural Science),2017,37(3):37-42.
[19]王引权,Schuchardt F,陈晖,等.翻堆频率对中药渣堆肥过程及其理化性质的影响[J].中国农学通报,2012,28(29):247-252.Wang Y Q,Schuchardt F,Chen H,et al. Effects of turning frequency on chemical and physical properties in windrow composting of spent Chinese herbal medicine[J]. Chinese Agricultural Science Bulletin,2012,28(29):247-252.
[20] 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.
[21]宿程远,郑鹏,阮祁华,等.中药渣与城市污泥好氧共堆肥的效能[J].环境科学,2016,37(10):4062-4068.Su C Y,Zhen P,Ruan Q H,et al. Efficiency of aerobic cocomposting of urban sludge and Chinese medicinal herbal residues[J]. Environmental Science,2016,37(10):4062-4068.
[22] Qian X,Sun W,Gu J,et al. Reducing antibiotic resistance genes,integrons,and pathogens in dairy manure by continuous thermophilic composting[J]. Bioresource Technology,2016,220:425-432.
[23] Ghosh S,Ramsden S J,La Para T M. The role of anaerobic digestion in controlling the release of tetracycline resistance genes and class 1 integrons from municipal wastewater treatment plants[J]. Applied Microbiology and Biotechnology,2009,84(4):791-796.
[24] Ma Y J,Wilson C A,Novak J T,et al. Effect of various sludge digestion conditions on sulfonamide,macrolide,and tetracycline resistance genes and class I integrons[J]. Environmental Science&Technology,2011,45(18):7855-7861.
[25] Zhang J Y,Chen M X,Sui Q W,et al. Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting[J]. Water Research,2016,91:339-349.
[26] Zhang L,Gu J,Wang X J, et al. Behavior of antibiotic resistance genes during co-composting of swine manure with Chinese medicinal herbal residues[J]. Bioresource Technology,2017,244:252-260.
[27] Wright G D. The antibiotic resistome:the nexus of chemical and genetic diversity[J]. Nature Reviews Microbiology,2007,5(3):175-186.
[28] Yang B,Meng L,Xue N D. Removal of five fluoroquinolone antibiotics during broiler manure composting[J]. Environmental Technology,2018,39(3):373-381.
[29] Selvam A,Xu D L,Zhao Z Y,et al. Fate of tetracycline,sulfonamide and fluoroquinolone resistance genes and the changes in bacterial diversity during composting of swine manure[J].Bioresource Technology,2012,126:383-390.
[30] Li J J, Xin Z H, Zhang Y Z, et al. Long-term manure application increased the levels of antibiotics and antibiotic resistance genes in a greenhouse soil[J]. Applied Soil Ecology,2017,121:193-200.
[31]崔二苹.生物质炭对粪肥堆肥过程中抗生素抗性基因行为特征的影响[D].杭州:浙江大学,2016. 38-43.Cui E P. The effect of biochar addition on antibiotic resistance genes during manure composting[D]. Hangzhou:Zhejiang University,2016. 38-43.
[32] Erickson M C,Liao J,Boyhan G,et al. Fate of manure-borne pathogen surrogates in static composting piles of chicken litter and peanut hulls[J]. Bioresource Technology,2010,101(3):1014-1020.
[33] Fang H,Wang H F,Cai L,et al. Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey[J].Environmental Science&Technology,2015,49(2):1095-1104.
[34] Skld O. Sulfonamide resistance:mechanisms and trends[J].Drug Resistance Updates,2000,3(3):155-160.
[35] Partridge S R,Tsafnat G,Coiera E,et al. Gene cassettes and cassette arrays in mobile resistance integrons[J]. FEMS Microbiology Reviews,2009,33(4):757-784.
[36] Hu H W,Wang J T,Li J,et al. Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils[J]. Environmental Microbiology,2016,18(11):3896-3909.
[37] Han X M,Hu H W,Shi X Z,et al. Impacts of reclaimed water irrigation on soil antibiotic resistome in urban parks of Victoria,Australia.[J]. Environmental Pollution,2016,211:48-57.
[38] Wang F H,Qiao M,Chen Z,et al. Antibiotic resistance genes in manure-amended soil and vegetables at harvest[J].Journal of Hazardous Materials,2015,299:215-221.
[39] 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.
[40] Rosser S J,Young H K. Identification and characterization of class 1 integrons in bacteria from an aquatic environment[J].Journal of Antimicrobial Chemotherapy,1999,44(1):11-18.
[41] Wang F H,Qiao M,Lv Z E,et al. Impact of reclaimed water irrigation on antibiotic resistance in public parks,Beijing,China[J]. Environmental Pollution,2014,184:247-253.
[42] Gillings M R,Krishnan S,Worden P J,et al. Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples[J]. FEMS Microbiology Letters,2008,287(1):56-62.
[43] He L Y,Liu Y S,Su H C,et al. Dissemination of antibiotic resistance genes in representative broiler feedlots environments:Identification of indicator ARGs and correlations with environmental variables[J]. Environmental Science&Technology,2014,48(22):13120-13129.
[44] Li X L,Shi L,Yang W Q,et al. New array of aacA4-catB3-dfrA1 gene cassettes and a noncoding cassette from a class-1-integron-positive clinical strain of Pseudomonas aeruginosa[J].Antimicrobial Agents and Chemotherapy,2006,50(6):2278-2279.
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