Please wait a minute...

Frontiers of Environmental Science & Engineering

Front. Environ. Sci. Eng.    2019, Vol. 13 Issue (3) : 35     https://doi.org/10.1007/s11783-019-1119-2
RESEARCH ARTICLE
Characteristics of two transferable aminoglycoside resistance plasmids in Escherichia coli isolated from pig and chicken manure
Chengjun Pu, Xiaoyan Gong, Ying Sun()
Beijing Key Laboratory of Farmland Soil Pollution Prevention and Remediation, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
Download: PDF(1726 KB)   HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

pRKZ3 is a non-conjugative IncQ plasmid, while pKANJ7 is a conjugative IncX plasmid.

The optimal mating time of pKANJ7 varied under different conditions.

Both of the two transferable ARPs had little impact on the growth of their hosts.

A relatively high level of fitness cost was observed for pKANJ7.

The fitness cost of ARPs depended on their hosts.

Plasmid-mediated antibiotic resistance genes (ARGs) have recently become a more prominent concern in the global environment. However, the prevalence of aminoglycoside resistance plasmids in the livestock industry is under reported. In this study, two transferable aminoglycoside resistance plasmids, pRKZ3 and pKANJ7, isolated from pig and chicken manure, were characterized. Results showed that pRKZ3 (8236 bp) is a non-conjugative IncQ plasmid and contains genes encoding for plasmid replication and stabilization (repA, repB and repC), mobilization (mob), and antibiotic resistance (arr-3 and aacA). pKANJ7 (30142 bp) is a conjugative IncX plasmid which codes for a type IV secretion system (T4SS). Conjugative transfer experiments showed that the optimal mating time of pKANJ7 was 8 h under the starvation condition, but the number of tranconjugants increased with time under the nutrient condition. Statistical analysis indicated that the two plasmids had little impact on the growth of their hosts, but a relatively high level of fitness cost due to pKANJ7 was observed. We also found that the fitness cost of plasmids depended on their hosts. Compared with pKANJ7, the relative fitness cost index of pRKZ3 varied within a narrow range during the 10 days of competition. The low level of fitness cost of pRKZ3 might contribute to the persistence of the plasmid in the environment. Our study provides new information for understanding the characterizations of antibiotic resistance plasmids (ARPs) in manure sources and helps to clarify the transfer and persistence of ARPs in the environment following the application of manure.

Keywords Escherichia coli      Characteristics      Aminoglycoside resistance plasmids      Transfer      Persistence     
This article is part of themed collection: Environmental Antibiotics and Antibiotic Resistance (Xin Yu, Hui Li & Virender K. Sharma)
Corresponding Authors: Ying Sun   
Issue Date: 29 April 2019
 Cite this article:   
Chengjun Pu,Xiaoyan Gong,Ying Sun. Characteristics of two transferable aminoglycoside resistance plasmids in Escherichia coli isolated from pig and chicken manure[J]. Front. Environ. Sci. Eng., 2019, 13(3): 35.
 URL:  
http://journal.hep.com.cn/fese/EN/10.1007/s11783-019-1119-2
http://journal.hep.com.cn/fese/EN/Y2019/V13/I3/35
Service
E-mail this article
E-mail Alert
RSS
Articles by authors
Chengjun Pu
Xiaoyan Gong
Ying Sun
Fig.1  Agarose gel electrophoresis of pRKZ3 (lane 1) and pKANJ7 (lane 2 and 3). Abbreviations: l, linear isoform; oc, open circular isoform; sc, supercoiled isoform.
Coding sequence Coordinates Strand Protein properties Similarity (%) Known or putative functions Accession
No.aa Mass(kDA)
repC 31–876 ? 281 30.9 96 initiation protein WP_011117304.1
repA 863–1702 ? 279 30.1 97 replication protein A WP_010904471.1
ORF3 1733–1939 ? 68 7.5 97 putative role in regulation of expression of repA and repC WP_011117302.1
repB 1996–2256 ? 86 9.8 95 primase WP_010895878.1
repB 2276–2551 ? 91 10.1 97 primase WP_010895878.1
arr-3 2679–3131 ? 150 17 100 NAD( + )–rifampin ADP-ribosyltransferase Arr-3 WP_001749986.1
aacA 3216–3869 ? 217 24.5 100 6'-N-acetyltransferase AAA25688.1
mob 3925–7248 ? 1107 122.6 100 mobilization protein WP_011117299.1
mob 7431–7691 + 86 9.8 100 mobilization protein WP_011117298.1
ORF10 7736–7894 + 52 5.5 ? ? ?
Tab.1  Annotation of predicted ORFs and the corresponding products of pRKZ3
Coding sequence Coordinates Strand Protein properties Similarity (%) Known or putative functions Accession
No.aa Mass(kDA)
stbD 1028–1279 + 83 9.2 100 plasmid stabilization protein WP_000121743.1
stbE 1269–1550 + 93 11.0 100 type II toxin-antitoxin system RelE/ParE family toxin WP_000220560.1
ORF3 1696–2019 + 107 12.2 100 hypothetical protein WP_001181903.1
ORF4 2052–2309 + 85 9.9 100 hypothetical protein WP_001328105.1
ORF5 2293–2514 + 73 8.2 100 hypothetical protein WP_001328106.1
ORF6 2607–2936 + 109 12.6 100 hypothetical protein WP_000866648.1
ORF7 3175–3372 + 65 7.4 100 hypothetical protein WP_001675595.1
ORF8 3523–3858 ? 111 12.5 100 hypothetical protein WP_001328108.1
ddp1 3981–4529 + 182 21.5 100 DNA distortion protein 1 WP_015058253.1
rlx 4532–4693 + 53 6.1 88 Relaxase WP_000538023.1
rlx 4684–5688 + 334 38.2 100 Relaxase WP_000538023.1
actX 5932–6540 + 202 23.8 100 transcription termination factor NusG WP_000872475.1
slt 6765–7409 + 214 23.9 100 transglycosylase WP_000953539.1
tivB2 7393–7683 + 96 10.7 100 P-type propilin WP_000921916.1
tivB3-4 7707–10466 + 919 104.8 100 T4SS ATPase WP_000108725.1
tivB5 10468–11205 + 245 27.7 100 pilus assembly WP_000737859.1
ORF17 11212–11475 + 87 9.8 100 hypothetical protein WP_001228869.1
tivB6 11487–12542 + 351 37.4 100 T4SS protein WP_000235774.1
tivB8 12732–13454 + 240 27.5 100 T4SS protein WP_000394570.1
tivB9 13460–14389 + 309 35.1 100 T4SS protein WP_000776689.1
tivB10 14386–15600 + 404 44.2 100 T4SS protein WP_001295061.1
tivB11 15618–16655 + 345 39.2 100 T4SS protein WP_000217791.1
cpl 16660–18495 + 611 69.2 100 T4SS Coupling protein WP_000053826.1
ORF24 18492–18887 + 131 14.8 100 hypothetical protein WP_000733627.1
ORF25 18890–19222 + 110 12.3 100 hypothetical protein WP_000699980.1
aph(3′)-Ia 19465–20280 + 271 30.9 100 aminoglycoside O-phosphotransferase APH(3′)-Ia WP_000018321.1
ORF27 20357–21232 + 291 32.3 96 short chain dehydrogenase WP_012478242.1
ORF28 21285–21653 + 122 13.6 63 ABC-F type ribosomal protection protein WP_013780328.1
IS26 21688–22404 + 238 28.5 100 IS6-like element IS26 family transposase WP_001398202.1
topB 22604–23641 + 345 37.4 100 type IA DNA topoisomerase WP_001235773.1
hns 23653–24102 + 149 17.5 100 DNA binding protein WP_001282381.1
ORF32 24186–24569 + 127 14.1 100 hypothetical protein WP_000059893.1
ORF33 24937–25575 ? 212 24.3 100 resolvase WP_024245155.1
parA 25861–26481 + 206 22.0 100 partitioning protein WP_000864791.1
parG 26533–26763 + 76 8.6 100 partitioning protein WP_000051064.1
ORF36 26779–27072 + 97 10.8 100 hypothetical protein WP_015060510.1
IS903 27074–28042 + 322 36.6 100 IS5-like element IS903B family transposase WP_000654804.1
ddp3 28102–28455 ? 117 13.6 100 DNA distortion polypeptide 3 WP_001467132.1
ORF39 28592–29038 ? 148 17.3 100 hypothetical protein WP_001074386.1
rep 29078–29812 ? 244 28.3 100 replication initiator protein WP_001050931.1
Tab.2  Annotation of predicted ORFs and the corresponding products of pKANJ7
Fig.2  The circular maps of pRKZ3 (A) and pKANJ7 (B). Genes marked with blue represent regions correlated with plasmid replication and stabilization. Genes marked with green or orange indicate regions correlated with plasmid transfer. Genes marked with red suggest regions involved in antibiotic resistance. Genes marked with gray or black indicate regions encoding for other/unknown functions.
Fig.3  Phylogenetic analysis of plasmids. The numbers on the tree indicate the percentages in the bootstrap analysis (1000 replications). The tree was reconstructed using the maximum composite likelihood method. Isolated plasmids in this study were marked with l.
Strains MIC of kanamycin (µg/mL)
E. coli DH5a 0.5
E. coli J53 1
E. coli DH5α ( + pRKZ3) 128
E. coli DH5a ( + pKANJ7) 256
E. coli J53 ( + pKANJ7) 1024
Tab.3  MICs of transformants and transconjugants
Fig.4  The number of donors, recipients and transconjugants (A) and conjugative transfer frequency (B) of pKANJ7 under the nutrient and starvation conditions. Error bars indicate standard deviations (n = 3).
Fig.5  Growth curves of E. coli DH5a carrying pRKZ3 and pKANJ7 (A), and E. coli J53 carrying pKANJ7 (B). Relative fitness cost index of pRKZ3 and pKANJ7 in E. coli DH5a (C) and pKANJ7 in E. coli J53 (D). Error bars indicate standard deviations (n = 3).
Strains µ Rµ
E. coli DH5a 0.71±0.0019 /
E. coli J53 0.72±0.0071 /
E. coli DH5a ( + pRKZ3) 0.69±0.0005 0.97±0.0007
E. coli DH5a ( + pKANJ7) 0.70±0.0027 0.98±0.0037
E. coli J53 ( + pKANJ7) 0.71±0.0025 0.99±0.0034
Tab.4  Growth rates (µ) and relative growth rates (Rµ) of E. coli at the exponential phase
1 LAndrup, L Smidt, KAndersen, LBoe (1998). Kinetics of conjugative transfer: A study of the plasmid pxo16 from bacillus thuringiensis subsp. Israelensis1. Plasmid, 40: 30–43
2 DBarilla, E Carmelo, FHayes (2007). The tail of the parG DNA segregation protein remodels parF polymers and enhances ATP hydrolysis via an arginine finger-like motif. Proceedings of the National Academy of Sciences of the United States of America, 104(6): 1811–1816
3 KBecker, S van Alen, E AIdelevich, NSchleimer, JSeggewi, AMellmann, UKaspar, GPeters (2018). Plasmid-encoded transferable mecb-mediated methicillin resistance in staphylococcus aureus. Emerging Infectious Diseases, 24(2): 242–248
4 ABeranek, M Zettl, KLorenzoni, ASchauer, MManhart, GKoraimann (2004). Thirty-eight c-terminal amino acids of the coupling protein TraD of the F-like conjugative resistance plasmid R1 are required and sufficient to confer binding to the substrate selector protein tram. Journal of Bacteriology, 186(20): 6999–7006
5 T L TBien, YSato-Takabe, MOgo, M Usui, SSuzuki (2015). Persistence of multi-drug resistance plasmids in sterile water under very low concentrations of tetracycline. Microbes and Environments, 30(4): 339–343
6 C TBinh, H Heuer, MKaupenjohann, KSmalla (2008). Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiology Ecology, 66: 25–37
7 ABousquet, S Henquet, FCompain, NGenel, GArlet, DDecré (2015). Partition locus-based classification of selected plasmids in Klebsiella pneumoniae, Escherichia coli and Salmonella enterica spp.: An additional tool. Journal of Microbiological Methods, 110: 85–91
8 ACarattoli, E Zankari, A García-Fernánde, L MVoldby, OLund, L Villa, A FMøller, HHasman (2014). In silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrobial Agents and Chemotherapy, 58(7): 3895–3903
9 LChen, H Y Hu, K D Chavda, S L Zhao, R K Liu, H Liang, WZhang, X MWang, M RJacobs, R ABonomo, B NKreiswirth (2014). Complete sequence of a KPC-producing INCN multidrug-resistant plasmid from an epidemic Escherichia coli sequence type 131 strain in China. Antimicrobial Agents and Chemotherapy, 58(4): 2422–2425
10 PChen, C Chen, XLi (2018). Transport of antibiotic resistance plasmids in porous media and the influence of surfactants. Frontiers of Environmental Science & Engineering, 12(2): 5
11 P JChristie, J P Vogel (2000). Bacterial type IV secretion: Conjugation systems adapted to deliver effector molecules to host cells. Trends in Microbiology, 8(8): 354–360
12 A MCoros, E Twiss, N PTavakoli, K MDerbyshire (2005). Genetic evidence that GTP is required for transposition of IS903 and Tn552 in Escherichia coli. Journal of Bacteriology, 187(13): 4598–4606
13 J LCottell, M A Webber, L J Piddock (2012). Persistence of transferable extended-spectrum-beta-lactamase resistance in the absence of antibiotic pressure. Antimicrobial Agents and Chemotherapy, 56(9): 4703–4706
14 B JDang, D Q Mao, Y Xu, YLuo (2017). Conjugative multi-resistant plasmids in Haihe River and their impacts on the abundance and spatial distribution of antibiotic resistance genes. Water Research, 111: 81–91
15 NDatta, P Kontomichalou (1965). Penicillinase synthesis controlled by infectious R factors in Enterobacteriaceae. Nature, 208:239–241
16 L LDevendec, G Mourand, SBougeard, JLéaustic, EJouy, A Keita, WCouet, NRousset, IKempf (2016). Impact of colistin sulfate treatment of broilers on the presence of resistant bacteria and resistance genes in stored or composted manure. Veterinary Microbiology, 194: 98–106
17 HDobiasova, M Dolejska (2016). Prevalence and diversity of IncX plasmids carrying fluoroquinolone and b-lactam resistance genes in Escherichia coli originating from diverse sources and geographical areas. Journal of Antimicrobial Chemotherapy, 71: 2118–2124
18 M LFoucault, P Courvalin, CGrillot-Courvalin (2009). Fitness cost of VanA-type vancomycin resistance in methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 53(6): 2354–2359
19 FGarnier, H Debat, MNadal (2018). Type IA DNA topoisomerases: A universal core and multiple activities. In: Drolet M, eds. DNA topoisomerases. Methods in Molecular Biology, 1703: 1–20.
20 MGiangrossi, K Wintraecken, RSpurio, R DVries (2014). Probing the relation between protein–protein interactions and DNA binding for a linker mutant of the bacterial nucleoid protein H-NS. Biochimica et Biophysica Acta, 1844: 339–345
21 NGoessweiner-Mohr, KArends, WKeller, EGrohmann (2014). Conjugation in gram-positive bacteria. Microbiology Spectrum, 2: 1–19
22 M TGuo, Q B Yuan, J Yang (2015). Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environmental Science & Technology, 49: 5771–5778
23 Q LGuo, A D Tomich, C L McElheny, V S Cooper, N Stoesser, MWang, NSluis-Cremer, YDoi (2016a). Glutathione-S-transferase FosA6 of Klebsiella pneumoniae origin conferring fosfomycin resistance in ESBL-producing Escherichia coli. Journal of Antimicrobial Chemotherapy, 71: 2460–2465
24 X YGuo, L J Hao, P Z Qiu, R Chen, JXu, X JKong, Z JShan, NWang (2016b). Pollution characteristics of 23 veterinary antibiotics in livestock manure and manure-amended soils in Jiangsu Province, China. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 51(6): 383–392
25 B CHaldorsen, G SSimonsen, ASundsfjord, ØSamuelsen (2014). Increased prevalence of aminoglycoside resistance in clinical isolates of Escherichia coli and Klebsiella spp. in Norway is associated with the acquisition of AAC(3)-II and AAC(6′)-Ib. Diagnostic Microbiology and Infectious Disease, 78: 66–69
26 EHarrison, M A Brockhurst (2012). Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends in Microbiology, 20(6): 262–267
27 EHarrison, D Guymer, A JSpiers, SPaterson, M ABrockhurst (2015). Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Current Biology, 25(15): 2034–2039
28 HHirt, K E Greenwood-Quaintance, M J Karau, L M Till, P C Kashyap, R Patel, G MDunny (2018). Enterococcus faecalis sex pheromone cCF10 enhances conjugative plasmid transfer in vivo. mBio, 9(1): 1–13
29 PHuang, Y Zhang, KXiao, FJiang, HWang, D Tang, DLiu, BLiu, Y Liu, XHe, HLiu, X Liu, ZQing, CLiu, J Huang, YRen, LYun, L Yin, QLin, CZeng, X Su, JYuan, LLin, N Hu, HCao, SHuang, YGuo, W Fan, JZeng (2018). The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome, 6(1): 1–17
30 HIto, H Ishii, MAkiba (2004). Analysis of the complete nucleotide sequence of an Actinobacillus pleuropneumoniae streptomycin–sulfonamide resistance plasmid, pMS260. Plasmid, 51: 41–47
31 T JJohnson, E M Bielak, D Fortini, L HHansen, HHasman, CDebroy, L KNolan, ACarattoli (2012). Expansion of the IncX plasmid family for improved identification and typing of novel plasmids in drug-resistant Enterobacteriaceae. Plasmid, 68: 43–50
32 S RJoy, S L Bartelt-Hunt, D D Snow, J E Gilley, B L Woodbury, D B Parker, D B Marx, X Li (2013). Fate and transport of antimicrobials and antimicrobial resistance genes in soil and runoff following land application of swine manure slurry. Environmental Science & Technology, 47: 12081–12088
33 NKassis-Chikhani, L Frangeul, LDrieux, CSengelin, VJarlier, SBrisse, GArlet, DDecré (2012). Complete nucleotide sequence of the first KPC-2- and SHV-12-encoding IncX plasmid, pKpS90, from Klebsiella pneumoniae. Antimicrobial Agents and Chemotherapy, 57(1): 618–620
34 Y HKe, Y F Wang, W F Li, Z L Chen (2015). Type IV secretion system of Brucella spp. and its effectors. Frontiers in Cellular and Infection Microbiology, 5: 1–10
35 AKottara, J P J Hall, E Harrison, M ABrockhurst (2017). Variable plasmid fitness effects and mobile genetic element dynamics across Pseudomonas species. FEMS Microbiology Ecology, 94(1): 1–7
36 VKrishnasamy, J Otte, ESilbergeld (2015). Antimicrobial use in Chinese swine and broiler poultry production. Antimicrobial Resistance and Infection Control, 4(17): 1–9
37 TKubori, M Koike, X TBui, SHigaki, S IAizawa, HNagai (2014). Native structure of a type IV secretion system core complex essential for Legionella pathogenesis. Proceedings of the National Academy of Sciences of the United States of America, 111(32): 11804–11809
38 I MLeon, S D Lawhon, K N Norman, D S Threadgill, N Ohta, JVinasco, H MScott (2018). Serotype diversity and antimicrobial resistance among Salmonella enterica isolates from patients at an equine referral hospital. Applied and Environmental Microbiology, 84(13): 1–15
39 RLi, H Zhu, JRuan, WQian, X Fang, ZShi, YLi, S Li, GShan, KKristiansen, SLi, H Yang, JWang, JWang (2010). De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20: 265–272
40 R CLi, L W Ye, Z W Zheng, E W C Chan, S Chen (2017). Genetic characterization of broad-host range IncQ plasmids harboring blaVEB-18 in vibrio species. Antimicrobial Agents and Chemotherapy, 61(7): 1–3
41 YLi, D Currie, A LZydney (2016). Enhanced purification of plasmid DNA isoforms by exploiting ionic strength effects during ultrafiltration. Biotechnology and Bioengineering, 113(4): 783–789
42 CLiu, H Zheng, MYang, ZXu, X Wang, LWei, BTang, F Liu, YZhang, YDing, X Tang, BWu, T JJohnson, HChen, C Tan (2015a). Genome analysis and in vivo virulence of porcine extraintestinal pathogenic Escherichia coli strain PCN033. BMC Genomics, 16: 1-18
43 C CLiu, H Y Kuo, C Y Tang, K C Chang, M L Liou (2014). Prevalence and mapping of a plasmid encoding a type IV secretion system in Acinetobacter baumannii. Genomics, 104: 215–223
44 Z BLiu, Z G Zhang, H Yan, J RLi, LShi (2015b). Isolation and molecular characterization of multidrug-resistant Enterobacteriaceae strains from pork and environmental samples in Xiamen, China. Journal of Food Protection, 78(1): 78–88
45 W ULo, K H Chow, P Y Law, K Y Ng, Y Y Cheung, E L Lai, P L Ho (2014). Highly conjugative IncX4 plasmids carrying bla CTX-M in Escherichia coli from humans and food animals. Journal of Medical Microbiology, 63: 835–840
46 WLoftie-Eaton, K Bashford, HQuinn, KDong, J Millstein, SHunter, M KThomason, HMerrikh, J MPonciano, E MTop (2017). Compensatory mutations improve general permissiveness to antibiotic resistance plasmids. Nature Ecology & Evolution, 1(9): 1354–1363
47 J SMadsen, L Riber, WKot, ABasfeld, MBurmølle, L HHansen, S JSørensen (2016). Type 3 fimbriae encoded on plasmids are expressed from a unique promoter without affecting host motility, facilitating an exceptional phenotype that enhances conjugal plasmid transfer. PLoS One, 11(9): 1–19
48 C WMcKinney, R S Dungan, A Moore, A BLeytem (2018). Occurrence and abundance of antibiotic resistance genes in agricultural soil receiving dairy manure. FEMS Microbiology Ecology, 94: 1–10
49 A SMillan, R Peña-Miller, MToll-Riera, Z VHalbert, A RMcLean, B SCooper, R CMacLean (2014). Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids. Nature Communications, 10(5): 1–11
50 D X FMollenkopf, J WStull, D AMathys, A SBowman, S MFeicht, S VGrooters, J BDaniels, T EWittum (2017). Carbapenemase-producing Enterobacteriaceae recovered from the environment of a swine farrow-to-finish operation in the United States. Antimicrobial Agents and Chemotherapy, 61(2): 1–9
51 HNakaminami, N Noguchi, SNishijima, IKurokawa, MSasatsu (2008). Characterization of the pTZ2162 encoding multidrug efflux gene qacB from Staphylococcus aureus. Plasmid, 60: 108–117
52 ANorman, L H Hansen, Q X She, S J Sørensen (2008). Nucleotide sequence of pOLA52: A conjugative IncX1 plasmid from Escherichia coli which enables biofilm formation and multidrug efflux. Plasmid, 60: 59–74
53 BNunez, P Avila, F D LCruz (1997). Genes involved in conjugative DNA processing of plasmid R6K. Molecular Microbiology, 24(6): 1157–1168
54 KOshima, H Nishida (2007). Phylogenetic relationships among Mycoplasmas based on the whole genomic information. Journal of Molecular Evolution, 65(3): 249–258
55 S RPartridge, J AEllem, S GTetu, Z YZong, I TPaulsen, J RIredell (2011). Complete sequence of pJIE143, apir-type plasmid carrying ISEcp1-blaCTX-M-15 from an Escherichia coli ST131 isolate. Antimicrobial Agents and Chemotherapy, 55(12): 5933–5935
56 J BPatel, F R Cockerill (2016). Performance standards for antimicrobial susceptibility testing. M100S, 26th ed
57 WPaulander, S Maisnier-Patin, D IAndersson (2009). The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and RpoS (sS). Genetics, 183: 539–546
58 SPeng, Y M Wang, B B Zhou, X G Lin (2015). Long-term application of fresh and composted manure increase tetracycline resistance in the arable soil of eastern China. Science of the Total Environment, 506–507: 279–286
59 GPérez-Segura, ÁPérez-Oseguera, M ACevallos (2013). The repAC replication system of the Rhizobium leguminosarum pRL7 plasmid is functional: Implications regarding the origin and evolution of repABC plasmids. Plasmid, 69: 49–57
60 APorse, K Schønning, CMunck, M O ASommer (2016). Survival and evolution of a large multidrug resistance plasmid in new clinical bacterial hosts. Molecular Biology and Evolution, 33(11): 2860–2873
61 C JPu, M H Lv, Y H Zeng, X Y Gong, Y Sun (2017). Drug resistance to four antibiotics of Escherichia coli in chicken and pig feces. Asian Journal of Ecotoxicology, 12(1): 141–147 (in Chinese)
62 XQian, J Gu, WSun, X JWang, J QSu, RStedfeld (2018). Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting. Journal of Hazardous Materials, 344: 716–722
63 Z GQiu, Y M Yu, Z L Chen, M Jin, DYan, Z GZhao, J FWang, Z QShen, X WWang, DQian, A H Huang, B C Zhang, J W Li (2012). Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera. Proceedings of the National Academy of Sciences of the United States of America, 109(13): 4944–4949
64 T ORahube, C K Yost (2012). Characterization of a mobile and multiple resistance plasmid isolated from swine manure and its detection in soil after manure application. Journal of Applied Microbiology, 112: 1123–1133
65 S ARakowski, M Filutowicz (2013). Plasmid R6K replication control. Plasmid, 69: 231–242
66 ARedzej, M Ukleja, SConnery, MTrokter, CFelisberto-Rodrigues, ACryar, KThalassinos, R DHayward, E VOrlova, GWaksman (2017). Structure of a VirD4 coupling protein bound to a VirB type IV secretion machinery. EMBO Journal, 36(20): 3080–3095
67 S CRibeiro, G A Monteiro, D M F Prazeres (2009). Evaluation of the effect of non-B DNA structures on plasmid integrity via accelerated stability studies. Journal of Pharmaceutical Sciences, 98(4): 1400–1408
68 N MRodriguez-Bonano, L JTorres-Bauza (2004). Molecular analysis of oriT and MobA protein in the 7.4kb mobilizable b-lactamase plasmid pSJ7.4 from Neisseria gonorrhoeae. Plasmid, 52(2): 89–101
69 MRysz, W R Mansfield, J D Fortner, P J J Alvarez (2013). Tetracycline resistance gene maintenance under varying bacterial growth rate, substrate and oxygen availability, and tetracycline concentration. Environmental Science & Technology, 47(13): 6995–7001
70 ASan Millan, S Garcia-Cobos, J AEscudero, LHidalgo, BGutierrez, LCarrilero, JCampos, BGonzalez-Zorn (2010). Haemophilus influenzae clinical isolates with plasmid pB1000 bearing blaROB-1: Fitness cost and interspecies dissemination. Antimicrobial Agents and Chemotherapy, 54(4): 1506–1511
71 A BScott, M Singh, JToribio, MHernandez-Jover, BBarnes, KGlass, BMoloney, ALee, P Groves (2017). Comparisons of management practices and farm design on Australian commercial layer and meat chicken farms: Cage, barn and free range. PLoS One, 12(11): 1–17
72 PShen, M L Yi, Y Fu, ZRuan, X XDu, Y SYu, X YXie (2017). Detection of an Escherichia coli sequence type 167 strain with two tandem copies of blaNDM-1 in the chromosome. Journal of Clinical Microbiology, 55(1): 199–204
73 FSilva, J A Queiroz, F C Domingues (2012). Evaluating metabolic stress and plasmid stability in plasmid DNA production by Escherichia coli. Biotechnology Advances, 30(3): 691–708
74 KSmalla, H Heuer, AGotz, DNiemeyer, EKrogerrecklenfort, ETietze (2000). Exogenous isolation of antibiotic resistance plasmids from piggery manure slurries reveals a high prevalence and diversity of IncQ-like plasmids. Applied and Environmental Microbiology, 66(11): 4854–4862
75 CSmillie, M P Garcillan-Barcia, M V Francia, E P C Rocha, F de la Cruz (2010). Mobility of plasmids. Microbiology and Molecular Biology Reviews, 74(3): 434–452
76 E TSumrall, E B Gallo, A O Aboderin, A Lamikanra, I NOkeke (2014). Dissemination of the transmissible quinolone-resistance gene qnrS1 by IncX plasmids in Nigeria. PLoS One, 9: e110279
77 JSun, X P Li, L X Fang, R Y Sun, Y Z He, J X Lin, X P Liao, Y J Feng, Y H Liu (2018). Co-occurrence of mcr-1 in the chromosome and on an IncHI2 plasmid: Persistence of colistin resistance in Escherichia coli. International Journal of Antimicrobial Agents, 51: 842–847
78 STokajian, R Moghnieh, TSalloum, HArabaghian, SAlousi, JMoussa, EAbboud, SYoussef, RHusni (2018). Extended-spectrum b-lactamase-producing Escherichia coli in wastewaters and refugee camp in Lebanon. Future Microbiology, 13(1): 81–95
79 S JUnterholzner, BHailer, BPoppenberger, WRozhon (2013). Characterisation of the stbD/E toxin–antitoxin system of pEP36, a plasmid of the plant pathogen Erwinia pyrifoliae. Plasmid, 70: 216–225
80 NWang, X Guo, JXu, XKong, S Gao, ZShan (2014). Pollution characteristics and environmental risk assessment of typical veterinary antibiotics in livestock farms in Southeastern China. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 49: 468–479
81 WWang, Z Baloch, Z XPeng, Y JHu, JXu, S Fanning, F XLi (2017). Genomic characterization of a large plasmid containing a blaNDM-1 gene carried on Salmonella enterica serovar Indiana C629 isolate from China. BMC Infectious Diseases, 17: 479
82 M EWetzel, G J Olsen, V Chakravartty, S KFarrand (2015). The repABC plasmids with quorum-regulated transfer systems in members of the Rhizobiales divide into two structurally and separately evolving groups. Genome Biology and Evolution, 7(12): 3337–3357
83 JWild, A Czyz, S ARakowski, MFilutowicz (2004). g Origin plasmids of R6K lineage replicate in diverse genera of Gram-negative bacteria. Annals of Microbiology, 54(4): 119–128
84 M HWong, E W Chan, S Chen (2017). IS26-mediated formation of a virulence and resistance plasmid in Salmonella Enteritidis. Journal of Antimicrobial Chemotherapy, 72(10): 2750–2754
85 J JYan, J J Wu, W C Ko, S H Tsai, C L Chuang, H M Wu, Y J Lu, J D Li (2004). Plasmid-mediated 16S rRNA methylases conferring high-level aminoglycoside resistance in Escherichia coli and Klebsiella pneumoniae isolates from two Taiwanese hospitals. Journal of Antimicrobial Chemotherapy, 54: 1007–1012
86 Y XYang, Y Q Yang, C W Lei, B H Liu, W Jiang, H NWang, M CGazitúa, A YZhang (2017). Characterization of pHeBE7, an IncFII-type virulence-resistance plasmid carrying bla CTX-M-98b, bla TEM-1, and rmtB genes, detected in Escherichia coli from a chicken isolate in China. Plasmid, 92: 37–42
87 M LZhang, S Chen, MGnegy, C SYe, W FLin, H RLin, XYu (2018). Environmental strains potentially contribute to the proliferation and maintenance of antibiotic resistance in drinking water: A case study of Cupriavidus metallidurans. Science of the Total Environment, 643: 819–826
88 NZhang, X Liu, RLiu, TZhang, MLi, Z R Zhang, Z T Qu, Z T Yuan, H C Yu (2019). Influence of reclaimed water discharge on the dissemination and relationships of sulfonamide, sulfonamide resistance genes along the Chaobai River, Beijing. Frontiers of Environmental Science & Engineering, 13(1): 1–12
89 QZhang, G Ying, CPan, YLiu, J Zhao (2015). Comprehensive evaluation of antibiotics emission and fate in the river basins of china: Source analysis, multimedia modeling, and linkage to bacterial resistance. Environmental Science & Technology, 49(11): 6772–6782
90 YZhang, A Z Gu, M He, DLi, J MChen (2016). Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environmental Science & Technology, 51: 570–580
Related articles from Frontiers Journals
[1] Yangyang Yu, Xiaolin Zhu, Guanlan Wu, Chengzhi Wang, Xing Yuan. Analysis of antibiotic resistance of Escherichia coli isolated from the Yitong River in North-east China[J]. Front. Environ. Sci. Eng., 2019, 13(3): 39-.
[2] Xuan Zhu, Chengsong Ye, Yuxin Wang, Lihua Chen, Lin Feng. Assessment of antibiotic resistance genes in dialysis water treatment processes[J]. Front. Environ. Sci. Eng., 2019, 13(3): 45-.
[3] Yifei Song, Lei Sun, Xinfeng Wang, Yating Zhang, Hui Wang, Rui Li, Likun Xue, Jianmin Chen, Wenxing Wang. Pollution characteristics of particulate matters emitted from outdoor barbecue cooking in urban Jinan in eastern China[J]. Front. Environ. Sci. Eng., 2018, 12(2): 14-.
[4] Shuai Wang, Tong Li, Chen Chen, Baicang Liu, John C. Crittenden. PVDF ultrafiltration membranes of controlled performance via blending PVDF-g-PEGMA copolymer synthesized under different reaction times[J]. Front. Environ. Sci. Eng., 2018, 12(2): 3-.
[5] Mengmeng Wang, Quanyin Tan, Joseph F. Chiang, Jinhui Li. Recovery of rare and precious metals from urban mines—A review[J]. Front. Environ. Sci. Eng., 2017, 11(5): 1-.
[6] Jianwei Liu, Kaixiong Yang, Lin Li, Jingying Zhang. A full-scale integrated-bioreactor with two zones treating odours from sludge thickening tank and dewatering house: performance and microbial characteristics[J]. Front. Environ. Sci. Eng., 2017, 11(4): 6-.
[7] Sheng Huang, Xin Zhao, Yanqiu Sun, Jianli Ma, Xiaofeng Gao, Tian Xie, Dongsheng Xu, Yi Yu, Youcai Zhao. Pollution of hazardous substances in industrial construction and demolition wastes and their multi-path risk within an abandoned pesticide manufacturing plant[J]. Front. Environ. Sci. Eng., 2017, 11(1): 12-.
[8] Feng ZHANG,Shengsong YU,Jie LI,Wenwei LI,Hanqing YU. Mechanisms behind the accelerated extracellular electron transfer in Geobacter sulfurreducens DL-1 by modifying gold electrode with self-assembled monolayers[J]. Front. Environ. Sci. Eng., 2016, 10(3): 531-538.
[9] Yuchen PANG,Jingjing HUANG,Jinying XI,Hongying HU,Yun ZHU. Effect of ultraviolet irradiation and chlorination on ampicillin-resistant Escherichia coli and its ampicillin resistance gene[J]. Front. Environ. Sci. Eng., 2016, 10(3): 522-530.
[10] Yanling WEI,Xunfei YIN,Lu QI,Hongchen WANG,Yiwei GONG,Yaqian LUO. Effects of carrier-attached biofilm on oxygen transfer efficiency in a moving bed biofilm reactor[J]. Front. Environ. Sci. Eng., 2016, 10(3): 569-577.
[11] Bing PEI,Hongyang CUI,Huan LIU,Naiqiang YAN. Chemical characteristics of fine particulate matter emitted from commercial cooking[J]. Front. Environ. Sci. Eng., 2016, 10(3): 559-568.
[12] Chao ZENG,Dongjie NIU,Youcai ZHAO. A comprehensive overview of rural solid waste management in China[J]. Front. Environ. Sci. Eng., 2015, 9(6): 949-961.
[13] Li SHENG,Shuhang HUANG,Minghao SUI,Lingdian ZHANG,Lei SHE,Yong CHEN. Deposition of copper nanoparticles on multiwalled carbon nanotubes modified with poly (acrylic acid) and their antimicrobial application in water treatment[J]. Front. Environ. Sci. Eng., 2015, 9(4): 625-633.
[14] Eunsung KAN,Chang-Il KOH,Kyunghyuk LEE,Joonwun KANG. Decomposition of aqueous chlorinated contaminants by UV irradiation with H2O2[J]. Front. Environ. Sci. Eng., 2015, 9(3): 429-435.
[15] Yi ZHAO,Tianxiang GUO,Zili ZANG. Activity and characteristics of “Oxygen-enriched” highly reactive absorbent for simultaneous flue gas desulfurization and denitrification[J]. Front. Environ. Sci. Eng., 2015, 9(2): 222-229.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed