Antibiotic-Induced, Increased Conjugative Transfer Is Common to Diverse Naturally Occurring ESBL Plasmids in Escherichia coli

Gang Liu, Karolina Bogaj, Valeria Bortolaia, John Elmerdahl Olsen, Line Elnif Thomsen*

*Corresponding author for this work

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Abstract

Previously, we showed that cefotaxime (CTX) exposure increases conjugative transfer of a bla CTX-M- 1 encoding IncI1 plasmid (IncI1/pST49/CTX-M-1) in Escherichia coli in a SOS-independent manner. This study aimed at investigating whether the observation was unique for that plasmid/strain/antibiotic combination or whether antibiotic-induced plasmid transfer (PT) is a more general phenomenon among plasmids in E. coli. Whole genome sequences of 25 E. coli strains were analyzed to identify different extended spectrum beta-lactamases (ESBL) plasmids enabling selection of a diverse collection of plasmids. Experiments were performed following exposure of these strains to 1/2 minimal inhibitory concentration (MIC) of CTX, ampicillin (AMP), or ciprofloxacin (CIP) before conjugation experiments. The frequency of PT was measured and compared to that of donors not exposed to antibiotics. Reverse-transcribed-quantitative real time polymerase chain reaction (RT-qPCR) was used to measure mRNA levels of five PT genes and two SOS response genes in donors exposed to antibiotics. The PT of eight strains (30.8% of strains tested) with IncI1/pST7/CTX-M-1, IncI1/pST49/CTX-M-1, IncI1/pST3/CTX-M-1, IncI1/pST293/CTX-M-1, IncI1/pST295/CTX-M-1, IncI1/pST16/CTX-M-55, and IncFII/CTX-M-14 (n = 2) plasmids was significantly increased following antibiotic exposure. CTX increased PT in all of these eight strain/plasmid combinations, AMP and CIP increased the PT in six and three strains, respectively. RT-qPCR showed that PT genes were up-regulated in the presence of the three antibiotics, whereas SOS-response genes were up-regulated only following CIP exposure. Our findings reveal that antibiotics can increase PT in E. coli strains with various ESBL plasmids. Thus, antibiotic-induced conjugative transfer of ESBL plasmids appears to be a common phenomenon in E. coli, having important implications for assessing the risks of antibiotic use.
Original languageEnglish
Article number2119
JournalFrontiers in Microbiology
Volume10
Number of pages12
ISSN1664-302X
DOIs
Publication statusPublished - 2019

Cite this

@article{666a6766f07444578eb4da58306ac17e,
title = "Antibiotic-Induced, Increased Conjugative Transfer Is Common to Diverse Naturally Occurring ESBL Plasmids in Escherichia coli",
abstract = "Previously, we showed that cefotaxime (CTX) exposure increases conjugative transfer of a bla CTX-M- 1 encoding IncI1 plasmid (IncI1/pST49/CTX-M-1) in Escherichia coli in a SOS-independent manner. This study aimed at investigating whether the observation was unique for that plasmid/strain/antibiotic combination or whether antibiotic-induced plasmid transfer (PT) is a more general phenomenon among plasmids in E. coli. Whole genome sequences of 25 E. coli strains were analyzed to identify different extended spectrum beta-lactamases (ESBL) plasmids enabling selection of a diverse collection of plasmids. Experiments were performed following exposure of these strains to 1/2 minimal inhibitory concentration (MIC) of CTX, ampicillin (AMP), or ciprofloxacin (CIP) before conjugation experiments. The frequency of PT was measured and compared to that of donors not exposed to antibiotics. Reverse-transcribed-quantitative real time polymerase chain reaction (RT-qPCR) was used to measure mRNA levels of five PT genes and two SOS response genes in donors exposed to antibiotics. The PT of eight strains (30.8{\%} of strains tested) with IncI1/pST7/CTX-M-1, IncI1/pST49/CTX-M-1, IncI1/pST3/CTX-M-1, IncI1/pST293/CTX-M-1, IncI1/pST295/CTX-M-1, IncI1/pST16/CTX-M-55, and IncFII/CTX-M-14 (n = 2) plasmids was significantly increased following antibiotic exposure. CTX increased PT in all of these eight strain/plasmid combinations, AMP and CIP increased the PT in six and three strains, respectively. RT-qPCR showed that PT genes were up-regulated in the presence of the three antibiotics, whereas SOS-response genes were up-regulated only following CIP exposure. Our findings reveal that antibiotics can increase PT in E. coli strains with various ESBL plasmids. Thus, antibiotic-induced conjugative transfer of ESBL plasmids appears to be a common phenomenon in E. coli, having important implications for assessing the risks of antibiotic use.",
author = "Gang Liu and Karolina Bogaj and Valeria Bortolaia and Olsen, {John Elmerdahl} and Thomsen, {Line Elnif}",
year = "2019",
doi = "10.3389/fmicb.2019.02119",
language = "English",
volume = "10",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A.",

}

Antibiotic-Induced, Increased Conjugative Transfer Is Common to Diverse Naturally Occurring ESBL Plasmids in Escherichia coli. / Liu, Gang; Bogaj, Karolina; Bortolaia, Valeria; Olsen, John Elmerdahl; Thomsen, Line Elnif.

In: Frontiers in Microbiology, Vol. 10, 2119, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Antibiotic-Induced, Increased Conjugative Transfer Is Common to Diverse Naturally Occurring ESBL Plasmids in Escherichia coli

AU - Liu, Gang

AU - Bogaj, Karolina

AU - Bortolaia, Valeria

AU - Olsen, John Elmerdahl

AU - Thomsen, Line Elnif

PY - 2019

Y1 - 2019

N2 - Previously, we showed that cefotaxime (CTX) exposure increases conjugative transfer of a bla CTX-M- 1 encoding IncI1 plasmid (IncI1/pST49/CTX-M-1) in Escherichia coli in a SOS-independent manner. This study aimed at investigating whether the observation was unique for that plasmid/strain/antibiotic combination or whether antibiotic-induced plasmid transfer (PT) is a more general phenomenon among plasmids in E. coli. Whole genome sequences of 25 E. coli strains were analyzed to identify different extended spectrum beta-lactamases (ESBL) plasmids enabling selection of a diverse collection of plasmids. Experiments were performed following exposure of these strains to 1/2 minimal inhibitory concentration (MIC) of CTX, ampicillin (AMP), or ciprofloxacin (CIP) before conjugation experiments. The frequency of PT was measured and compared to that of donors not exposed to antibiotics. Reverse-transcribed-quantitative real time polymerase chain reaction (RT-qPCR) was used to measure mRNA levels of five PT genes and two SOS response genes in donors exposed to antibiotics. The PT of eight strains (30.8% of strains tested) with IncI1/pST7/CTX-M-1, IncI1/pST49/CTX-M-1, IncI1/pST3/CTX-M-1, IncI1/pST293/CTX-M-1, IncI1/pST295/CTX-M-1, IncI1/pST16/CTX-M-55, and IncFII/CTX-M-14 (n = 2) plasmids was significantly increased following antibiotic exposure. CTX increased PT in all of these eight strain/plasmid combinations, AMP and CIP increased the PT in six and three strains, respectively. RT-qPCR showed that PT genes were up-regulated in the presence of the three antibiotics, whereas SOS-response genes were up-regulated only following CIP exposure. Our findings reveal that antibiotics can increase PT in E. coli strains with various ESBL plasmids. Thus, antibiotic-induced conjugative transfer of ESBL plasmids appears to be a common phenomenon in E. coli, having important implications for assessing the risks of antibiotic use.

AB - Previously, we showed that cefotaxime (CTX) exposure increases conjugative transfer of a bla CTX-M- 1 encoding IncI1 plasmid (IncI1/pST49/CTX-M-1) in Escherichia coli in a SOS-independent manner. This study aimed at investigating whether the observation was unique for that plasmid/strain/antibiotic combination or whether antibiotic-induced plasmid transfer (PT) is a more general phenomenon among plasmids in E. coli. Whole genome sequences of 25 E. coli strains were analyzed to identify different extended spectrum beta-lactamases (ESBL) plasmids enabling selection of a diverse collection of plasmids. Experiments were performed following exposure of these strains to 1/2 minimal inhibitory concentration (MIC) of CTX, ampicillin (AMP), or ciprofloxacin (CIP) before conjugation experiments. The frequency of PT was measured and compared to that of donors not exposed to antibiotics. Reverse-transcribed-quantitative real time polymerase chain reaction (RT-qPCR) was used to measure mRNA levels of five PT genes and two SOS response genes in donors exposed to antibiotics. The PT of eight strains (30.8% of strains tested) with IncI1/pST7/CTX-M-1, IncI1/pST49/CTX-M-1, IncI1/pST3/CTX-M-1, IncI1/pST293/CTX-M-1, IncI1/pST295/CTX-M-1, IncI1/pST16/CTX-M-55, and IncFII/CTX-M-14 (n = 2) plasmids was significantly increased following antibiotic exposure. CTX increased PT in all of these eight strain/plasmid combinations, AMP and CIP increased the PT in six and three strains, respectively. RT-qPCR showed that PT genes were up-regulated in the presence of the three antibiotics, whereas SOS-response genes were up-regulated only following CIP exposure. Our findings reveal that antibiotics can increase PT in E. coli strains with various ESBL plasmids. Thus, antibiotic-induced conjugative transfer of ESBL plasmids appears to be a common phenomenon in E. coli, having important implications for assessing the risks of antibiotic use.

U2 - 10.3389/fmicb.2019.02119

DO - 10.3389/fmicb.2019.02119

M3 - Journal article

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 2119

ER -