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Frontiers of Environmental Science & Engineering

Front. Environ. Sci. Eng.    2019, Vol. 13 Issue (3) : 35
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
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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.
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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
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