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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

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Front. Environ. Sci. Eng.    2022, Vol. 16 Issue (3) : 32    https://doi.org/10.1007/s11783-021-1466-7
RESEARCH ARTICLE
Antibiotic resistome mostly relates to bacterial taxonomy along a suburban transmission chain
Ziyan Qin1, Qun Gao1(), Qiang Dong2, Joy D. Van Nostrand3, Qi Qi1, Yifan Su1, Suo Liu1, Tianjiao Dai1, Jingmin Cheng1, Jizhong Zhou3,4,5, Yunfeng Yang1()
1. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China
2. Institute of Chemical Defense, Beijing 102205, China
3. Institute for Environmental Genomics, and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA
4. School of Civil Engineering and Environmental Sciences, University of Oklahoma, Norman, OK 73019, USA
5. Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA
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Abstract

• The α-diversities of resistome were lower in manure and compost than in soils.

• There were significant correlations between the resistome and bacterial taxonomy.

• Bacterial taxonomy was the highest in explaining resistome variances.

Antibiotic resistance genes comprising antibiotic resistome are of great concern due to their increase in the environment. Recent evidence of shared resistomes between soils and animal husbandry has imposed potential risks to human health. However, the correlation between a given community’s resistome and bacterial taxonomic composition is controversial. Here, a transmission chain of resistomes from swine manure to compost and compost-amended soil were analyzed in five suburban areas of Beijing, China, with unamended agricultural soils as control soils. Antibiotic resistomes and bacterial taxonomic compositions were distinct between (I) manure and compost; and (II) compost-amended and control soils. In manure, compost, and compost-amended soils, the β-diversity of the resistome and bacterial taxonomic composition was significantly correlated, while no correlation was detected in control soils. Bacterial taxonomic composition explained 36.0% of total variations of the resistome composition, much higher than environmental factors. Together, those results demonstrated that antibiotic resistome was closely related to bacterial taxonomic composition along the suburban transmission chain.

Keywords Antibiotic resistance genes      Resistome      Bacterial taxonomy      Transmission chain     
Corresponding Author(s): Qun Gao,Yunfeng Yang   
Issue Date: 13 July 2021
 Cite this article:   
Ziyan Qin,Qun Gao,Qiang Dong, et al. Antibiotic resistome mostly relates to bacterial taxonomy along a suburban transmission chain[J]. Front. Environ. Sci. Eng., 2022, 16(3): 32.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-021-1466-7
https://academic.hep.com.cn/fese/EN/Y2022/V16/I3/32
Fig.1  Heatmaps of the (a) resistome and (b) bacterial phyla in manure, compost, compost-amended soil, and control soil, with 80 samples in total. The scale represents the relative abundance of each ARG or each bacterial phylum, which was normalized as a Z score detailed in the method.
Group Treatment PERMANOVAa) MRPP ANOSIM
R2 P δ P R P
Resistomec) Sample types 0.425 0.001b) 0.169 0.001 0.549 0.001
Sample sites 0.074 0.001 0.216 0.067 0.032 0.082
Bacterial taxonomic composition Sample types 0.321 0.001 0.715 0.001 0.735 0.001
Sample sites 0.106 0.001 0.821 0.001 0.065 0.022
Tab.1  Non-parametric multivariate dissimilarity analyses of resistome and bacterial taxonomic composition
Fig.2  Pearson correlations between richness (a), Shannon index (b), Simpson index (c), and β-diversity (based on Bray-Curtis dissimilarity) (d) of ARGs and bacterial OTUs. The significance of the correlation was determined by P<0.050. There are 80 samples in total.
Types Indices r P
Manure Richness 0.145 0.543
Shannon index 0.211 0.372
Simpson index 0.215 0.363
β-diversity 0.346 <0.001a)
Compost Richness 0.441 0.059
Shannon index 0.284 0.238
Simpson index 0.107 0.663
β-diversity 0.430 <0.001
Compost-amended Soil Richness −0.163 0.493
Shannon index −0.069 0.773
Simpson index −0.164 0.489
β-diversity 0.318 <0.001
Control Soil Richness −0.029 0.902
Shannon index −0.146 0.540
Simpson index −0.050 0.835
β-diversity −0.018 0.808
Tab.2  Pearson correlations between richness, Shannon index, Simpson index, and β-diversity (based on Bray-Curtis dissimilarity) of ARGs and bacterial OTUs in manure, compost, compost-amended soil, and control soil
Fig.3  Significant positive Pearson correlation pairs between bacterial genera and resistome in the group of (a) manure, (b) compost, (c) compost-amended soil, and (d) control soil samples. The thickness of the edge represents correlation values. Green circles represent bacterial genus. Pink circles represent resistome. The size of the circle represents the degree of connectedness. The significance of the correlation was determined by P<0.050.
Influence factors All Samples Manure Compost Compost-amended Soil Control Soil
R2a) coef
(R2 = 0.445)
R2 coef
(R2 = 0.230)
R2 coef
(R2 = 0.228)
R2 coef
(R2 = 0.118)
R2 coef
(R2 = 0.027)
Bacterial taxonomic composition 0.360***b) 0.286*** 0.120** 0.064* 0.185*** 0.086* 0.101*** 0.107*** 0.0003 0.026
Sample Type 0.025*** −0.004
Sample Site 0.002 −0.002 0.145*** 0.027** 0.075** 0.006 0.006 −0.003 0.008 −0.007
Temperature 0.003 −0.010** 0.022 0.002 0.057 0.005 0.001 −0.004 0.0004 0.003
Moisture 0.195*** 0.018*** 0.026 −0.016 0.064* 0.011 0.004 0.0001 0.014 −0.007
Tab.3  Contribution of bacterial taxonomic composition and environmental factors in shaping the resistome by multiple regression on distance matrices (MRM) in all samples, manure, compost, compost-amended soil, and control soil
1 R E Alcock, A Sweetman, K C Jones (1999). Assessment of organic contanhnant fate in waste water treatment plants I: Selected compounds and physicochemical properties. Chemosphere, 38(10): 2247–2262
https://doi.org/10.1016/S0045-6535(98)00444-5
2 M J Anderson (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1): 32–46
3 F Caméléna, B Pilmis, B Mollo, A Hadj, A Le Monnier, A Mizrahi (2016). Infections caused by Tissierella praeacuta: A report of two cases and literature review. Anaerobe, 40: 15–17
https://doi.org/10.1016/j.anaerobe.2016.04.015
4 R Cao, J Wang, W Ben, Z Qiang (2020). The profile of antibiotic resistance genes in pig manure composting shaped by composting stage: Mesophilic-thermophilic and cooling-maturation stages. Chemosphere, 250: 126181
https://doi.org/10.1016/j.chemosphere.2020.126181
5 Q L Chen, X L An, B X Zheng, M Gillings, J Peñuelas, L Cui, J Q Su, Y G Zhu (2019). Loss of soil microbial diversity exacerbates spread of antibiotic resistance. Soil Ecology Letters, 1(1–2): 3–13
https://doi.org/10.1007/s42832-019-0011-0
6 D de Oliveira-Garcia, M Dall’agnol, M Rosales, A C Azzuz, M B Martinez, J A Giron (2002). Characterization of flagella produced by clinical strains of Stenotrophomonas maltophilia. Emerging Infectious Diseases, 8(9): 918–923
https://doi.org/10.3201/eid0809.010535
7 T Fernandes, I Vaz-Moreira, C M Manaia (2019). Neighbor urban wastewater treatment plants display distinct profiles of bacterial community and antibiotic resistance genes. Environmental Science and Pollution Research International, 26(11): 11269–11278
https://doi.org/10.1007/s11356-019-04546-y
8 K J Forsberg, S Patel, M K Gibson, C L Lauber, R Knight, N Fierer, G Dantas (2014). Bacterial phylogeny structures soil resistomes across habitats. Nature, 509(7502): 612–616
https://doi.org/10.1038/nature13377
9 K J Forsberg, A Reyes, B Wang, E M Selleck, M O Sommer, G Dantas (2012). The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337(6098): 1107–1111
https://doi.org/10.1126/science.1220761
10 Q Gao, Q Dong, L Wu, Y Yang, L Hale, Z Qin, C Xie, Q Zhang, J D Van Nostrand, J Zhou (2020). Environmental antibiotics drives the genetic functions of resistome dynamics. Environment International, 135: 105398
https://doi.org/10.1016/j.envint.2019.105398
11 S Ghosh, T M LaPara (2007). The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME Journal, 1(3): 191–203
https://doi.org/10.1038/ismej.2007.31
12 S Ghosh, M Sadowsky, M Roberts, J Gralnick, T LaPara (2009). Sphingobacterium sp. strain PM2‐P1‐29 harbours a functional tet (X) gene encoding for the degradation of tetracycline. Journal of Applied Microbiology, 106(4): 1336–1342
https://doi.org/10.1111/j.1365-2672.2008.04101.x
13 M R Gillings, H W Stokes (2012). Are humans increasing bacterial evolvability? Trends in Ecology & Evolution, 27(6): 346–352
https://doi.org/10.1016/j.tree.2012.02.006
14 H J Hong, M I Hutchings, M J Buttner (2008).Vancomycin resistance VanS/VanR two-component systems. In: Utsumi R, ed. Bacterial Signal Transduction: Networks and Drug Targets. New York: Springer New York, 200–213
15 B Huerta, E Marti, M Gros, P Lopez, M Pompeo, J Armengol, D Barcelo, J L Balcazar, S Rodriguez-Mozaz, R Marce (2013). Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Science of the Total Environment, 456–457: 161–170
https://doi.org/10.1016/j.scitotenv.2013.03.071
16 S Jechalke, H Heuer, J Siemens, W Amelung, K Smalla (2014). Fate and effects of veterinary antibiotics in soil. Trends in Microbiology, 22(9): 536–545
https://doi.org/10.1016/j.tim.2014.05.005
17 S Jechalke, C Kopmann, I Rosendahl, J Groeneweg, V Weichelt, E Krogerrecklenfort, N Brandes, M Nordwig, G C Ding, J Siemens, H Heuer, K Smalla (2013). Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Applied and Environmental Microbiology, 79(5): 1704–1711
https://doi.org/10.1128/AEM.03172-12
18 Q K Ji C H , Zhang D , Li (2020). Influences and mechanisms of nanofullerene on the horizontal transfer of plasmid-encoded antibiotic resistance genes between E. coli strains. Frontiers of Environmental Science & Engineering, 14(6): 108
19 U Klümper, L Riber, A Dechesne, A Sannazzarro, L H Hansen, S J Sorensen, B F Smets (2015). Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community. ISME Journal, 9(4): 934–945
https://doi.org/10.1038/ismej.2014.191
20 T Kusakizako, H Miyauchi, R Ishitani, O Nureki (2020). Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochimica et Biophysica Acta, 1862(12): 183154
https://doi.org/10.1016/j.bbamem.2019.183154
21 S O Leclercq, C Wang, Z Sui, H Wu, B Zhu, Y Deng, J Feng (2016). A multiplayer game: Species of Clostridium, Acinetobacter, and Pseudomonas are responsible for the persistence of antibiotic resistance genes in manure-treated soils. Environmental Microbiology, 18(10): 3494–3508
https://doi.org/10.1111/1462-2920.13337
22 P Legendre, L Legendre (2012). Numerical Ecology. Amsterdam,AE: Elsevier
23 H Liao, V P Friman, S Geisen, Q Zhao, P Cui, X Lu, Z Chen, Z Yu, S Zhou (2019). Horizontal gene transfer and shifts in linked bacterial community composition are associated with maintenance of antibiotic resistance genes during food waste composting. Science of the Total Environment, 660: 841–850
https://doi.org/10.1016/j.scitotenv.2018.12.353
24 J W Lichstein (2007). Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecology, 188(2): 117–131
https://doi.org/10.1007/s11258-006-9126-3
25 T Liu, S K Awasthi, Y Duan, Z Zhang, M K Awasthi (2020). Effect of fine coal gasification slag on improvement of bacterial diversity community during the pig manure composting. Bioresource Technology, 304: 123024
https://doi.org/10.1016/j.biortech.2020.123024
26 T Looft, T A Johnson, H K Allen, D O Bayles, D P Alt, R D Stedtfeld, W J Sul, T M Stedtfeld, B Chai, J R Cole, S A Hashsham, J M Tiedje, T B Stanton (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proceedings of the National Academy of Sciences of the United States of America, 109(5): 1691–1696
https://doi.org/10.1073/pnas.1120238109
27 X Ma, Q Zhang, M Zheng, Y Gao, T Yuan, L Hale, J D Van Nostrand, J Zhou, S Wan, Y Yang (2019). Microbial functional traits are sensitive indicators of mild disturbance by lamb grazing. ISME Journal, 13(5): 1370–1373
https://doi.org/10.1038/s41396-019-0354-7
28 T Magoč, S L Salzberg (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics (Oxford, England), 27(21): 2957–2963
https://doi.org/10.1093/bioinformatics/btr507
29 R N Mannanov, R K Sattarova (2001). Antibiotics produced by Bacillus bacteria. Chemistry of Natural Compounds, 37(2): 117–123
https://doi.org/10.1023/A:1012314516354
30 B M Marshall, S B Levy (2011). Food animals and antimicrobials: impacts on human health. Clinical Microbiology Reviews, 24(4): 718–733
https://doi.org/10.1128/CMR.00002-11
31 E Martinez, S Djordjevic, H Stokes, P R Chowdhury (2013).Lateral Gene Transfer in Evolution. RamatAviv: Springer, 79–103
32 M Mendez, I H Huang, K Ohtani, R Grau, T Shimizu, M R Sarker (2008). Carbon catabolite repression of type IV pilus-dependent gliding motility in the anaerobic pathogen Clostridium perfringens. Journal of Bacteriology, 190(1): 48–60
https://doi.org/10.1128/JB.01407-07
33 V Neubauer, E Humer, E Mann, I Kroger, N Reisinger, M Wagner, Q Zebeli, R M Petri (2019). Effects of clay mineral supplementation on particle-associated and epimural microbiota, and gene expression in the rumen of cows fed high-concentrate diet. Anaerobe, 59: 38–48
https://doi.org/10.1016/j.anaerobe.2019.05.003
34 S S Pao, I T Paulsen, M H Saier Jr (1998). Major facilitator superfamily. Microbiology and Molecular Biology Reviews, 62(1): 1–34
https://doi.org/10.1128/MMBR.62.1.1-34.1998
35 F Peng, Y Guo, A Isabwe, H Chen, Y Wang, Y Zhang, Z Zhu, J Yang (2020). Urbanization drives riverine bacterial antibiotic resistome more than taxonomic community at watershed scale. Environment International, 137: 105524
https://doi.org/10.1016/j.envint.2020.105524
36 A Pruden, M Arabi, H N Storteboom (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46(21): 11541–11549
https://doi.org/10.1021/es302657r
37 M Qiao, W Chen, J Su, B Zhang, C Zhang (2012). Fate of tetracyclines in swine manure of three selected swine farms in China. Journal of Environmental Sciences-China, 24(6): 1047–1052
https://doi.org/10.1016/S1001-0742(11)60890-5
38 M Schweizer, G V Bloemberg, C Graf, A L Falkowski, P Ochsner, P Graber, S Urffer, D Goldenberger, V Hinic, S Graf, P E Tarr (2016). Chronic osteomyelitis due to Tissierella carlieri: First case. Open Forum Infectious Diseases, 3(1): ofw012
https://doi.org/10.1093/ofid/ofw012
39 J F Jr Siqueira, I N Rôças (2006).Catonella morbi and Granulicatella adiacens: new species in endodontic infections. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics, 102(2): 259–264
https://doi.org/10.1016/j.tripleo.2005.09.021
40 J F Jr Siqueira, I N Rôças (2008). Update on endodontic microbiology: candidate pathogens and patterns of colonisation. Endodontic Practice Today, 2(1): 7–20
41 C S Smillie, M B Smith, J Friedman, O X Cordero, L A David, E J Alm (2011). Ecology drives a global network of gene exchange connecting the human microbiome. Nature, 480(7376): 241–244
https://doi.org/10.1038/nature10571
42 H W Stokes, M R Gillings (2011). Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiology Reviews, 35(5): 790–819
https://doi.org/10.1111/j.1574-6976.2011.00273.x
43 J Q Su, X L An, B Li, Q L Chen, M R Gillings, H Chen, T Zhang, Y G Zhu (2017). Metagenomics of urban sewage identifies an extensively shared antibiotic resistome in China. Microbiome, 5(1): 1–15
https://doi.org/10.1186/s40168-017-0298-y
44 W Tao, X X Zhang, F Zhao, K Huang, H Ma, Z Wang, L Ye, H Ren (2016). High levels of antibiotic resistance genes and their correlations with bacterial community and mobile genetic elements in pharmaceutical wastewater treatment bioreactors. PLoS One, 11(6): e0156854
https://doi.org/10.1371/journal.pone.0156854
45 K J Towner (2009). Acinetobacter: an old friend, but a new enemy. Journal of Hospital Infection, 73(4): 355–363
https://doi.org/10.1016/j.jhin.2009.03.032
46 N Udikovic-Kolic, F Wichmann, N A Broderick, J Handelsman (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
https://doi.org/10.1073/pnas.1409836111
47 Q Wang, G M Garrity, J M Tiedje, J R Cole (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267
https://doi.org/10.1128/AEM.00062-07
48 L Wu, Y Yang, S Chen, Z Jason Shi, M Zhao, Z Zhu, S Yang, Y Qu, Q Ma, Z He, J Zhou, Q He (2017). Microbial functional trait of rRNA operon copy numbers increases with organic levels in anaerobic digesters. ISME Journal, 11(12): 2874–2878
https://doi.org/10.1038/ismej.2017.135
49 N Wu, W Y Zhang, S Y Xie, M Zeng, H X Liu, J H Yang, X Y Liu, F Yang (2020). Increasing prevalence of antibiotic resistance genes in manured agricultural soils in northern China. Frontiers of Environmental Science & Engineering, 14(1): 1
50 N Yan (2013). Structural advances for the major facilitator superfamily (MFS) transporters. Trends in Biochemical Sciences, 38(3): 151–159
https://doi.org/10.1016/j.tibs.2013.01.003
51 H Zhang, H He, S Chen, T Huang, K Lu, Z Zhang, R Wang, X Zhang, H Li (2019). Abundance of antibiotic resistance genes and their association with bacterial communities in activated sludge of wastewater treatment plants: Geographical distribution and network analysis. Journal of Environmental Sciences-China, 82: 24–38
https://doi.org/10.1016/j.jes.2019.02.023
52 J Zhang, Q Gao, Q Zhang, T Wang, H Yue, L Wu, J Shi, Z Qin, J Zhou, J Zuo, Y Yang (2017). Bacteriophage–prokaryote dynamics and interaction within anaerobic digestion processes across time and space. Microbiome, 5(1): 1–10
https://doi.org/10.1186/s40168-017-0272-8
53 M Zhang, L Y He, Y S Liu, J L Zhao, J N Zhang, J Chen, Q Q Zhang, G G Ying (2020). Variation of antibiotic resistome during commercial livestock manure composting. Environment International, 136: 105458
https://doi.org/10.1016/j.envint.2020.105458
54 T Zhang, M Zhang, X Zhang, H H Fang (2009). Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environmental Science & Technology, 43(10): 3455–3460
https://doi.org/10.1021/es803309m
55 D Zhu, H T Wang, F Zheng, X R Yang, P Christie, Y G Zhu (2019). Collembolans accelerate the dispersal of antibiotic resistance genes in the soil ecosystem. Soil Ecology Letters, 1(1–2): 14–21
https://doi.org/10.1007/s42832-019-0002-1
56 Y G Zhu, T A Johnson, J Q Su, M Qiao, G X Guo, R D Stedtfeld, S A Hashsham, J M Tiedje (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
https://doi.org/10.1073/pnas.1222743110
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