Characteristics of two transferable aminoglycoside resistance plasmids in <i>Escherichia coli</i> isolated from pig and chicken manure

doi:10.1007/s11783-019-1119-2

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

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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

Corresponding Author(s): 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:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1119-2
https://academic.hep.com.cn/fese/EN/Y2019/V13/I3/35

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.

Tab.1 Annotation of predicted ORFs and the corresponding products of pRKZ3

Coding sequence	Coordinates	Strand	Protein properties		Similarity (%)	Known or putative functions	Accession
Coding sequence	Coordinates	Strand	No.aa	Mass(kDA)	Similarity (%)	Known or putative functions	Accession
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.

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).

Tab.4 Growth rates (µ) and relative growth rates (R_µ) of E. coli at the exponential phase

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