Effect of fertilizer types on antibiotic resistance genes and bacterial community in vegetable fields
-
摘要: 农田土壤生态系统是抗生素抗性基因(ARGs)的源与汇, 畜禽粪便施用是土壤中ARGs的重要来源。畜禽粪便在蔬菜地土壤中的大量施用, 加剧了蔬菜地土壤ARGs的污染, 对人类健康造成潜在危害。本文采集了河北省不同施肥类型(施用鲜鸡粪、鲜羊粪、鲜牛粪、商品有机肥以及单施化肥)的蔬菜地表层土壤(0~20 cm)样品, 采用定量PCR技术和高通量测序技术对蔬菜地土壤ARGs和细菌群落结构开展了研究, 旨在探究不同施肥类型蔬菜地土壤中ARGs的分布特征及其影响因素。结果表明, 不同施肥类型蔬菜地土壤中均检测到较高丰度的四环素类ARGs (tetA、tetC、tetG、tetL、tetO、tetM、tetW、tetQ)、磺胺类ARGs (sul1、sul2)以及Ⅰ类整合酶基因(intI1), 其中所有施肥处理土壤中磺胺类ARGs总绝对丰度高达9.96×109 copies∙g−1(干土), 且显著高于四环素类ARGs总丰度[1.07×109 copies∙g−1(干土)]。畜禽粪肥和化肥的施用都显著增加了土壤中ARGs丰度, 其中高化肥施加量土壤中ARGs检出丰度最高[6.34×109 copies∙g−1(干土)], 商品有机肥土壤中ARGs检出丰度最低[3.09×108 copies∙g−1(干土)]。施畜禽粪肥土壤中细菌群落的Shannon指数和Chao1指数显著高于高化肥施加量土壤, 但与低化肥施加量土壤差异不显著, 说明畜禽粪肥施用显著提高了土壤细菌群落的α多样性。Pearson相关性分析结果表明, 细菌群落结构是影响ARGs分布的重要因素。IntI1基因与sul2、tetG、tetQ以及tetW基因呈显著正相关(P<0.05), 说明intI1基因在ARGs的传播和扩散中也起着重要作用。本研究结果表明高化肥施用量能显著增加蔬菜地土壤ARGs的丰度, 商品有机肥的施用对土壤ARGs丰度影响最小。本研究为评估不同施肥类型蔬菜地土壤中ARGs的污染现状提供了相应的数据参考。Abstract: Farmland ecosystems are essential sources and sinks of antibiotic resistance genes (ARGs), and the application of livestock manure is a major contributor to ARGs in soil. The massive application of livestock manure to vegetable fields has intensified the pollution caused by ARGs in soil. Raw consumption of edible vegetables is one of the most direct ways to introduce ARGs from the soil–plant system to humans, which poses a potential threat to human health. However, few studies have investigated the effects of different fertilizer types on ARGs and bacterial communities in vegetable fields. In this study, 21 soil samples (0–20 cm) were collected from vegetable fields in Hebei Province using different fertilizer types (fresh fowl manure, fresh sheep manure, fresh cattle manure, commercial organic fertilizer, and chemical fertilizer). The distributions and characteristics of ARGs and bacterial communities in vegetable fields were investigated using real-time quantitative polymerase chain reaction (PCR) and high-throughput sequencing techniques. Eight tetracycline resistance genes (tetA, tetC, tetG, tetL, tetO, tetM, tetW, and tetQ), two sulfonamide resistance genes (sul1 and sul2), and one intI1 gene were detected in all vegetable fields. The absolute abundance of sulfonamide resistance genes (9.96×109 copies·g−1 in dry soil) was significantly higher than that of tetracycline resistance genes (1.07×109 copies·g−1 in dry soil). The application of livestock manure and chemical fertilizer both significantly increased the abundance of ARGs in vegetable fields. The highest abundance of ARGs (6.34×109 copies∙g−1 in dry soil) was found in vegetable fields with higher chemical fertilizer amendment, while the lowest abundance of ARGs (3.09×108 copies∙g−1 in dry soil) was found in vegetable soil with commercial organic fertilizer. In addition, the Shannon and Chao1 indices, representing the α diversity of the soil bacterial community, were significantly higher in soil fertilized with livestock manure compared to high-chemical fertilizer application but not in low-chemical fertilization soil, indicating that livestock manure application significantly increased the abundance and diversity of the soil bacterial community. Pearson’s correlation analysis showed that soil bacterial community structure was an important factor influencing the distribution of ARGs. Proteobacteriota, Bacteroidota, Actinobacteriota, and Firmicutes were the dominant potential hosts of ARGs and were significantly correlated with sulfonamide and tetracycline resistance genes (P<0.05). The distribution of ARGs was also affected by soil organic matter and total nitrogen content. The intI1 gene had significant and positive correlations with the sul2, tetG, tetQ, and tetW genes, suggesting its crucial role in ARGs dissemination. In the present study, the use of higher concentrations of chemical fertilizers led to a significantly increased abundance of ARGs in the soil of vegetable fields, whereas the application of commercial organic fertilizers had the least effect on ARGs abundance. This study serves as a guide for evaluating the status of ARGs pollution in vegetable fields with different fertilizer types.
-
![]()
图 1 不同施肥类型蔬菜地土壤中sul1、sul2、tetA、tetC、tetG、tetL、tetO、tetM、tetW、tetQ和intI1基因的绝对丰度(a)及土壤环境因子与抗性基因丰度间的冗余分析(b)
Figure 1. Absolute abundances of sul1, sul2, tetA, tetC, tetG, tetL, tetO, tetM, tetW, tetQ and intI1 genes in soils under different fertilization treatments (a) and redundancy analysis of absolute abundance of antibiotic resistance genes and soil environmental factors (b)
![]()
图 2 不同施肥类型蔬菜地土壤中细菌优势门(相对丰度>1%)的相对丰度(a)和基于Bray-Curtis距离(NMDS)的细菌群落结构组成(b)
Figure 2. Relative abundance of bacterial dominance phyla (relative abundance > 1%) in soils (a) and structural composition of the bacterial community based on Bray-Curtis distance (NMDS) (b) under different fertilization treatments
![]()
图 3 不同施肥处理土壤细菌α多样性
Figure 3. Soil bacterial α diversity under different fertilization treatments
![]()
图 4 土壤细菌α多样性与土壤环境因子Pearson相关性(a)和主要细菌门与抗性基因的Pearson相关性(b)
Figure 4. Pearson’s correlation of soil bacterial α diversity and environmental factors (a) and Pearson’s correlation of major bacterial phyla with antibiotic resistance genes (b)
表 1 采样点信息
Table 1 Details of soil sampling sites
处理
Treatment采样地
Sampling site经纬度
Longitude and latitude种植面积
Planting area (hm2)蔬菜种类
Vegetable type种植年限
Planting years (a)施肥量
Fertilizer application rate (t∙hm−2)施肥种类
Fertilizer typeOF 定州市
Dingzhou City115°13′N, 38°33′E 0.09 西红柿
Tomato6 30 商品有机肥
Commercial organic fertilizerSM 定州市
Dingzhou City114°95′N, 38°63′E 0.10 韭菜
Leek1 75 鲜羊粪
Fresh sheep manureCM1 涞水县
Laishui County115°71′N, 39°33′E 0.07 生菜
Romaine lettuce6 45 鲜牛粪
Fresh cattle manureCM2 安新县
Anxin County115°92′N, 38°87′E 0.10 白菜
Chinese cabbage5 84 鲜牛粪
Fresh cattle manureFM 清苑区
Qingyuan District115°57′N, 38°86′E 0.03 芹菜
Celery20 52.5 鲜鸡粪
Fresh fowl manureCF1 清苑区
Qingyuan District115°33′N, 38°48′E 0.20 芹菜
Celery10 0.825 化肥
Chemical fertilizerCF2 安新县
Anxin County115°93′N, 38°87′E 0.08 西红柿
Tomato6 3 化肥
Chemical fertilizer
下载: 导出CSV
表 2 不同施肥类型下土壤环境因子分析
Table 2 Physical and chemical properties of soil under different fertilization treatments
处理
Treatment土壤含水量
Soil water content (%)土壤有机质
Soil organic matter content (g·kg−1)pH 土壤总氮
Total nitrogen (g·kg−1)OF 18.70±0.42c 15.74±0.02cd 7.11±0.07c 0.07±0.01cd SM 7.98±1.48e 20.01±0.68bc 7.39±0.05ab 0.11±0.03bc CM1 14.44±1.84d 24.99±0.44b 7.28±0.05b 0.12±0.02b CM2 21.37±1.35b 25.25±0.16b 7.49±0.05a 0.14±0.01b FM 20.81±1.17bc 23.42±0.32b 7.28±0.06b 0.13±0.02b CF1 13.00±2.02d 18.45±0.32bd 7.48±0.01a 0.10±0.01bd CF2 26.83±0.41a 33.99±0.59a 7.06±0.11c 0.22±0.05a 不同处理详情见表1。不同小写字母代表各处理间差异显著(P<0.05)。Details of each treatment can be seen in Table 1. Different lowercase letters indicate significant differences among treatments (P<0.05).
下载: 导出CSV
表 3 抗性基因、intI1基因和土壤环境因子的Pearson相关性分析
Table 3 Pearson’s correlation analysis among antibiotic resistance genes, intI1 gene and soil environmental factors
sul1 sul2 tetA tetC tetG tetL tetM tetO tetQ tetW intI1 SOM SWC pH TN sul2 0.84* tetA 0.31 0.19 tetC −0.35 −0.36 0.77* tetG 0.50 0.74 0.53 0.23 tetL 0.40 0.43 0.59 0.34 0.53 tetM 0.10 0.21 0.73 0.68 0.56 0.90** tetO −0.44 −0.09 0.07 0.40 0.50 0.07 0.32 tetQ 0.77* 0.96** 0.19 −0.29 0.81* 0.38 0.22 0.07 tetW 0.79* 0.94** 0.12 −0.38 0.67 0.62 0.34 −0.08 0.89** intI1 0.65 0.93** 0.32 −0.09 0.90** 0.55 0.45 0.23 0.93** 0.88** SOM 0.52 0.82* 0.18 −0.11 0.83* 0.67 0.54 0.33 0.86* 0.90** 0.92** SWC 0.25 0.23 0.83* 0.65 0.55 0.17 0.40 0.11 0.31 0.01 0.35 0.12 pH −0.75 −0.62 −0.16 0.31 −0.53 0.07 0.23 0.05 −0.69 −0.46 −0.47 −0.33 −0.34 TN 0.60 0.89** 0.26 −0.12 0.83* 0.69 0.55 0.22 0.87* 0.93** 0.96** 0.97** 0.16 −0.32 SWC表示含水率; SOM表示土壤有机质; TN表示总氮。*和**分别表示在P<0.05和P<0.01水平显著相关。SWC is soil water content, SOM is soil organic matter content, TN is total nitrogen content. * and ** indicate significant correlation at P<0.05 and P<0.01 levels, respectively.
下载: 导出CSV
-
[1] QIAO M, YING G G, SINGER A C, et al. Review of antibiotic resistance in China and its environment[J]. Environment International, 2018, 110: 160−172 doi: 10.1016/j.envint.2017.10.016
[2] MARTINEZ J L. Environmental pollution by antibiotics and by antibiotic resistance determinants[J]. Environmental Pollution, 2009, 157(11): 2893−2902 doi: 10.1016/j.envpol.2009.05.051
[3] 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
[4] 安新丽, 苏建强. 土壤抗生素抗性组: 来源、扩散和驱动因子[J]. 科技导报, 2022, 40(3): 64−74 AN X L, SU J Q. The soil resistome: origin, dissemination and driving factor[J]. Science & Technology Review, 2022, 40(3): 64−74
[5] 2020年中国兽用抗菌药使用情况报告[N]. 北京: 中国畜牧兽医报, 2021-11-14 (003) Report on the use of veterinary antibiotics in China in 2020[N]. Beijing: Chinese Animal Husbandry and Veterinary News, 2021-11-14 (003)
[6] CHEE-SANFORD J C, MACKIE R I, KOIKE S, et al. Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste[J]. Journal of Environmental Quality, 2009, 38(3): 1086−1108 doi: 10.2134/jeq2008.0128
[7] 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
[8] HEUER H, SCHMITT H, SMALLA K. Antibiotic resistance gene spread due to manure application on agricultural fields[J]. Current Opinion in Microbiology, 2011, 14(3): 236−243 doi: 10.1016/j.mib.2011.04.009
[9] FRANZ E, VAN BRUGGEN A H C. Ecology of E. coli O157: H7 and Salmonella enterica in the primary vegetable production chain[J]. Critical Reviews in Microbiology, 2008, 34(3/4): 143−161
[10] JI X L, SHEN Q H, LIU F, et al. Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai, China[J]. Journal of Hazardous Materials, 2012, 235: 178−185
[11] MCKINNEY C W, DUNGAN R S, MOORE A, et al. Occurrence and abundance of antibiotic resistance genes in agricultural soil receiving dairy manure[J]. FEMS Microbiology Ecology, 2018, 94(3): fiy010
[12] HEUER H, SOLEHATI Q, ZIMMERLING U, et al. Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine[J]. Applied and Environmental Microbiology, 2011, 77(7): 2527−2530 doi: 10.1128/AEM.02577-10
[13] CHENG J H, TANG X Y, CUI J F. Distinct aggregate stratification of antibiotic resistome in farmland soil with long-term manure application[J]. Science of the Total Environment, 2022, 833: 155088 doi: 10.1016/j.scitotenv.2022.155088
[14] 苏志国, 张衍, 代天娇, 等. 环境中抗生素抗性基因与Ⅰ型整合子的研究进展[J]. 微生物学通报, 2018, 45(10): 2217−2233 SU Z G, ZHANG Y, DAI T J, et al. Antibiotic resistance genes and class Ⅰ integron in the environment: research progress[J]. Microbiology China, 2018, 45(10): 2217−2233
[15] 沈怡雯, 黄智婷, 谢冰. 抗生素及其抗性基因在环境中的污染、降解和去除研究进展[J]. 应用与环境生物学报, 2015, 21(2): 181−187 SHEN Y W, HUANG Z T, XIE B. Advances in research of pollution, degradation and removal of antibiotics and antibiotic resistance genes in the environment[J]. Chinese Journal of Applied and Environmental Biology, 2015, 21(2): 181−187
[16] MU Q H, LI J, SUN Y X, et al. Occurrence of sulfonamide-, tetracycline-, plasmid-mediated quinolone- and macrolide-resistance genes in livestock feedlots in Northern China[J]. Environmental Science and Pollution Research, 2015, 22(9): 6932−6940 doi: 10.1007/s11356-014-3905-5
[17] LI T T, LI R C, CAO Y F, et al. Soil antibiotic abatement associates with the manipulation of soil microbiome via long-term fertilizer application[J]. Journal of Hazardous Materials, 2022, 439: 129704 doi: 10.1016/j.jhazmat.2022.129704
[18] WANG F H, SUN R B, HU H W, et al. The overlap of soil and vegetable microbes drives the transfer of antibiotic resistance genes from manure-amended soil to vegetables[J]. Science of the Total Environment, 2022, 828: 154463 doi: 10.1016/j.scitotenv.2022.154463
[19] PU Q, ZHAO L X, LI Y T, et al. Manure fertilization increase antibiotic resistance in soils from typical greenhouse vegetable production bases, China[J]. Journal of Hazardous Materials, 2020, 391: 122267 doi: 10.1016/j.jhazmat.2020.122267
[20] 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 doi: 10.1016/j.jhazmat.2015.05.028
[21] 鲍士旦. 土壤农化分析[M]. 3版. 北京: 中国农业出版社, 2000 BAO S D. Soil and Agricultural Chemistry Analysis[M]. 3rd ed. Beijing: China Agriculture Press, 2000
[22] AMINOV R I, GARRIGUES-JEANJEAN N, MACKIE R I. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins[J]. Applied and Environmental Microbiology, 2001, 67(1): 22−32 doi: 10.1128/AEM.67.1.22-32.2001
[23] SUZUKI M T, TAYLOR L T, DELONG E F. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5’-nuclease assays[J]. Applied and Environmental Microbiology, 2000, 66(11): 4605−4614 doi: 10.1128/AEM.66.11.4605-4614.2000
[24] WALTERS W, HYDE E R, BERG-LYONS D, et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys[J]. mSystems, 2016, 1(1): e00009−e00015
[25] BOLYEN E, RIDEOUT J R, DILLON M R, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2[J]. Nature Biotechnology, 2019, 37(9): 1091
[26] GLÖCKNER F O, YILMAZ P, QUAST C, et al. 25 years of serving the community with ribosomal RNA gene reference databases and tools[J]. Journal of Biotechnology, 2017, 261: 169−176 doi: 10.1016/j.jbiotec.2017.06.1198
[27] BOKULICH N A, KAEHLER B D, RIDEOUT J R, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin[J]. Microbiome, 2018, 6: 90 doi: 10.1186/s40168-018-0470-z
[28] 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 doi: 10.1016/j.soilbio.2018.04.009
[29] 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 doi: 10.1128/AEM.01682-13
[30] ZHAO L, DONG Y H, WANG H. Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China[J]. Science of the Total Environment, 2010, 408(5): 1069−1075 doi: 10.1016/j.scitotenv.2009.11.014
[31] 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 doi: 10.1016/j.apsoil.2017.10.007
[32] 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 doi: 10.1016/j.jhazmat.2017.11.020
[33] WU N, ZHANG W Y, XIE S Y, et al. Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China[J]. Frontiers of Environmental Science & Engineering, 2020, 14(1): 1
[34] 钱勋. 好氧堆肥对畜禽粪便中抗生素抗性基因的削减条件探索及影响机理研究[D]. 杨凌: 西北农林科技大学, 2016 QIAN X. Study on the conditions of reducing antibiotic resistance genes in livestock manure by aerobic composting and its influencing mechanism[D]. Yangling: Northwest A & F University, 2016
[35] ZHAO X, WANG J H, ZHU L S, et al. Environmental analysis of typical antibiotic-resistant bacteria and ARGs in farmland soil chronically fertilized with chicken manure[J]. Science of the Total Environment, 2017, 593: 10−17
[36] SUNDSTRÖM L, RÅDSTRÖM P, SWEDBERG G, et al. Site-specific recombination promotes linkage between trimethoprim resistance and sulfonamide resistance genes. Sequence characterization of dhfrV and sulI and a recombination active locus of Tn21[J]. Molecular and General Genetics MGG, 1988, 213(2/3): 191−201
[37] 韩婉雪, 王凤花, 柏兆海, 等. 畜禽粪便堆放地土壤中抗生素抗性基因和细菌群落的垂直分布特征[J]. 中国生态农业学报(中英文), 2022, 30(2): 268−275 HAN W X, WANG F H, BAI Z H, et al. Vertical distribution of antibiotic resistance genes and bacterial communities in soil of livestock manure stacking site[J]. Chinese Journal of Eco-Agriculture, 2022, 30(2): 268−275
[38] 张宇亭. 长期施肥对土壤微生物多样性和抗生素抗性基因累积的影响[D]. 重庆: 西南大学, 2017 ZHANG Y T. Effects of long-term fertilization on soil microbial diversity and antibiotic resistance gene accumulation[D]. Chongqing: Southwest University, 2017
[39] ANGERS D A, CHANTIGNY M H, MACDONALD J D, et al. Differential retention of carbon, nitrogen and phosphorus in grassland soil profiles with long-term manure application[J]. Nutrient Cycling in Agroecosystems, 2010, 86(2): 225−229 doi: 10.1007/s10705-009-9286-3
[40] MAILLARD É, ANGERS D A. Animal manure application and soil organic carbon stocks: a meta-analysis[J]. Global Change Biology, 2014, 20(2): 666−679 doi: 10.1111/gcb.12438
[41] ZHONG W H, GU T, WANG W, et al. The effects of mineral fertilizer and organic manure on soil microbial community and diversity[J]. Plant and Soil, 2010, 326(1/2): 511−522
[42] CHINNADURAI C, GOPALASWAMY G, BALACHANDAR D. Long term effects of nutrient management regimes on abundance of bacterial genes and soil biochemical processes for fertility sustainability in a semi-arid tropical Alfisol[J]. Geoderma, 2014, 232: 563−572
[43] SUN R B, ZHANG X X, GUO X S, et al. Bacterial diversity in soils subjected to long-term chemical fertilization can be more stably maintained with the addition of livestock manure than wheat straw[J]. Soil Biology and Biochemistry, 2015, 88: 9−18 doi: 10.1016/j.soilbio.2015.05.007
[44] KUMAR U, NAYAK A K, SHAHID M, et al. Continuous application of inorganic and organic fertilizers over 47 years in paddy soil alters the bacterial community structure and its influence on rice production[J]. Agriculture, Ecosystems & Environment, 2018, 262: 65−75
[45] WANG Q F, JIANG X, GUAN D W, et al. Long-term fertilization changes bacterial diversity and bacterial communities in the maize rhizosphere of Chinese Mollisols[J]. Applied Soil Ecology, 2018, 125: 88−96 doi: 10.1016/j.apsoil.2017.12.007
[46] ZHOU Z C, ZHENG J, WEI Y Y, et al. Antibiotic resistance genes in an urban river as impacted by bacterial community and physicochemical parameters[J]. Environmental Science and Pollution Research, 2017, 24(30): 23753−23762 doi: 10.1007/s11356-017-0032-0
[47] WANG F H, HAN W X, CHEN S M, et al. Fifteen-year application of manure and chemical fertilizers differently impacts soil ARGs and microbial community structure[J]. Frontiers in Microbiology, 2020, 11: 62 doi: 10.3389/fmicb.2020.00062
[48] AWASTHI M K, LIU T, CHEN H Y, et al. The behavior of antibiotic resistance genes and their associations with bacterial community during poultry manure composting[J]. Bioresource Technology, 2019, 280: 70−78 doi: 10.1016/j.biortech.2019.02.030
[49] ZHANG R M, LIU X, WANG S L, et al. Distribution patterns of antibiotic resistance genes and their bacterial hosts in pig farm wastewater treatment systems and soil fertilized with pig manure[J]. Science of the Total Environment, 2021, 758: 143654 doi: 10.1016/j.scitotenv.2020.143654
[50] MA L P, LI A D, YIN X L, et al. The prevalence of integrons as the carrier of antibiotic resistance genes in natural and man-made environments[J]. Environmental Science & Technology, 2017, 51(10): 5721−5728
[51] 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 doi: 10.1016/j.envpol.2013.08.038
计量
- 文章访问数: 271
- HTML全文浏览量: 166
- PDF下载量: 79
