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Published in: Gut Pathogens 1/2018

Open Access 01-12-2018 | Research

ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost

Authors: Amit Ranjan, Julia Scholz, Torsten Semmler, Lothar H. Wieler, Christa Ewers, Stefanie Müller, Derek J. Pickard, Peter Schierack, Karsten Tedin, Niyaz Ahmed, Katharina Schaufler, Sebastian Guenther

Published in: Gut Pathogens | Issue 1/2018

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Abstract

Background

Extended spectrum beta lactamase (ESBL)-producing extraintestinal pathogenic Escherichia coli infections are of global interest because of their clinical and economic impact. The ESBL resistance genes disseminate through plasmids, and are found in successful global lineages such as ST131 and ST648. The carriage of plasmids has been suggested to result in a fitness burden, but recently it was shown that ESBL-plasmids enhanced virulence in pandemic ST131 and ST648 lineages without affecting their fitness. Herein, we investigated the influence of ESBL-plasmids on bacterial competition and serum resistance, both of which are essential characteristics of ExPEC during infections.

Methods

Triplets of ESBL-plasmid-carrying wildtype (WT), plasmid-cured variant (PCV) and transformant (T) of five ExPEC strains of ST131 and ST648 were used for bacterial competition experiments with colicin-producing commensal E. coli, competitive adhesion experiments and serum survival. In addition, resilience after SDS, acid, osmotic challenges and RNA sequence data were analyzed.

Results

In all five strains tested, ESBL-plasmid carriage did not negatively influence E. coli fitness in direct bacterial competition with commensal E. coli in vitro. That is, WTs did not show any disadvantages when compared to their isogenic plasmid-free PCV. For one strain we even found the opposite as PCV17433 was out-competed by a commensal strain, which suggests an even protective role of the ESBL-plasmid carried by the WT17433. Similarly, in the serum-resistance experiments, the PCVs of two strains (PCV17433 and PCV17887) were more sensitive to serum, unlike WTs and Ts. The observed inter-strain differences could be explained by the different genetic content of plasmids carried in those strains.

Conclusions

Overall, we found no compelling evidence for an increased burden resulting from the carriage of ESBL-plasmids in the absence of antimicrobial selection pressure in the strains of pandemic ST131 and ST648; rather, the possession of certain ESBL-plasmids was beneficial for some strains in regarding competition fitness and serum survival.
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Literature
2.
go back to reference Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123–40.CrossRefPubMed Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123–40.CrossRefPubMed
3.
go back to reference Ranjan A, et al. Comparative genomics of Escherichia coli isolated from skin and soft tissue and other extraintestinal infections. MBio. 2017;8(4):e01070-17.CrossRefPubMedPubMedCentral Ranjan A, et al. Comparative genomics of Escherichia coli isolated from skin and soft tissue and other extraintestinal infections. MBio. 2017;8(4):e01070-17.CrossRefPubMedPubMedCentral
4.
go back to reference Dho-Moulin M, Fairbrother JM. Avian pathogenic Escherichia coli (APEC). Vet Res. 1999;30(2–3):299–316.PubMed Dho-Moulin M, Fairbrother JM. Avian pathogenic Escherichia coli (APEC). Vet Res. 1999;30(2–3):299–316.PubMed
5.
go back to reference Russo TA, Johnson JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microb Infect. 2003;5(5):449–56.CrossRef Russo TA, Johnson JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microb Infect. 2003;5(5):449–56.CrossRef
6.
go back to reference Shaikh S, et al. Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J Biol Sci. 2015;22(1):90–101.CrossRefPubMed Shaikh S, et al. Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J Biol Sci. 2015;22(1):90–101.CrossRefPubMed
7.
go back to reference Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565–91.CrossRefPubMedPubMedCentral Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565–91.CrossRefPubMedPubMedCentral
8.
go back to reference de Been M, et al. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 2014;10(12):e1004776.CrossRefPubMedPubMedCentral de Been M, et al. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 2014;10(12):e1004776.CrossRefPubMedPubMedCentral
9.
go back to reference Ewers C, et al. CTX-M-15-D-ST648 Escherichia coli from companion animals and horses: another pandemic clone combining multiresistance and extraintestinal virulence? J Antimicrob Chemother. 2014;69(5):1224–30.CrossRefPubMed Ewers C, et al. CTX-M-15-D-ST648 Escherichia coli from companion animals and horses: another pandemic clone combining multiresistance and extraintestinal virulence? J Antimicrob Chemother. 2014;69(5):1224–30.CrossRefPubMed
10.
go back to reference Ranjan A, et al. Genomic and functional portrait of a highly virulent, CTX-M-15-producing H30-Rx subclone of Escherichia coli sequence type 131. Antimicrob Agents Chemother. 2015;59(10):6087–95.CrossRefPubMedPubMedCentral Ranjan A, et al. Genomic and functional portrait of a highly virulent, CTX-M-15-producing H30-Rx subclone of Escherichia coli sequence type 131. Antimicrob Agents Chemother. 2015;59(10):6087–95.CrossRefPubMedPubMedCentral
11.
go back to reference Guenther S, Ewers C, Wieler LH. Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol. 2011;2:246.CrossRefPubMedPubMedCentral Guenther S, Ewers C, Wieler LH. Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol. 2011;2:246.CrossRefPubMedPubMedCentral
13.
go back to reference Clermont O, et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother. 2009;64(2):274–7.CrossRefPubMed Clermont O, et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother. 2009;64(2):274–7.CrossRefPubMed
14.
go back to reference Johnson JR, Johnston BD, Gordon DM. Rapid and specific detection of the Escherichia coli sequence type 648 complex within phylogroup F. J Clin Microbiol. 2017;55(4):1116–21.CrossRefPubMedPubMedCentral Johnson JR, Johnston BD, Gordon DM. Rapid and specific detection of the Escherichia coli sequence type 648 complex within phylogroup F. J Clin Microbiol. 2017;55(4):1116–21.CrossRefPubMedPubMedCentral
16.
go back to reference Hirai I, et al. Detection of chromosomal blaCTX-M-15 in Escherichia coli O25b-B2-ST131 isolates from the Kinki region of Japan. Int J Antimicrob Agents. 2013;42(6):500–6.CrossRefPubMed Hirai I, et al. Detection of chromosomal blaCTX-M-15 in Escherichia coli O25b-B2-ST131 isolates from the Kinki region of Japan. Int J Antimicrob Agents. 2013;42(6):500–6.CrossRefPubMed
17.
go back to reference Rodriguez I, et al. Chromosomal location of blaCTX-M genes in clinical isolates of Escherichia coli from Germany, The Netherlands and the UK. Int J Antimicrob Agents. 2014;43(6):553–7.CrossRefPubMed Rodriguez I, et al. Chromosomal location of blaCTX-M genes in clinical isolates of Escherichia coli from Germany, The Netherlands and the UK. Int J Antimicrob Agents. 2014;43(6):553–7.CrossRefPubMed
18.
go back to reference Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol. 2010;8(4):260–71.CrossRefPubMed Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol. 2010;8(4):260–71.CrossRefPubMed
19.
go back to reference Crossman LC, et al. A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J Bacteriol. 2010;192(21):5822–31.CrossRefPubMedPubMedCentral Crossman LC, et al. A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J Bacteriol. 2010;192(21):5822–31.CrossRefPubMedPubMedCentral
20.
go back to reference Schaufler K, et al. Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages. Front Microbiol. 2016;7:336.CrossRefPubMedPubMedCentral Schaufler K, et al. Carriage of extended-spectrum beta-lactamase-plasmids does not reduce fitness but enhances virulence in some strains of pandemic E. coli lineages. Front Microbiol. 2016;7:336.CrossRefPubMedPubMedCentral
21.
go back to reference Schaufler K, et al. ESBL-plasmids carrying toxin-antitoxin systems can be “cured” of wild-type Escherichia coli using a heat technique. Gut Pathog. 2013;5(1):34.CrossRefPubMedPubMedCentral Schaufler K, et al. ESBL-plasmids carrying toxin-antitoxin systems can be “cured” of wild-type Escherichia coli using a heat technique. Gut Pathog. 2013;5(1):34.CrossRefPubMedPubMedCentral
22.
go back to reference Bano S, et al. Pattern of induction of colicin E9 synthesis by sub MIC of Norfloxacin antibiotic. Microbiol Res. 2013;168(10):661–6.CrossRefPubMed Bano S, et al. Pattern of induction of colicin E9 synthesis by sub MIC of Norfloxacin antibiotic. Microbiol Res. 2013;168(10):661–6.CrossRefPubMed
24.
go back to reference Nandanwar N, et al. Extraintestinal pathogenic Escherichia coli (ExPEC) of human and avian origin belonging to sequence type complex 95 (STC95) portray indistinguishable virulence features. Int J Med Microbiol. 2014;304(7):835–42.CrossRefPubMed Nandanwar N, et al. Extraintestinal pathogenic Escherichia coli (ExPEC) of human and avian origin belonging to sequence type complex 95 (STC95) portray indistinguishable virulence features. Int J Med Microbiol. 2014;304(7):835–42.CrossRefPubMed
25.
go back to reference Wang Y. The function of OmpA in Escherichia coli. Biochem Biophys Res Commun. 2002;292(2):396–401.CrossRefPubMed Wang Y. The function of OmpA in Escherichia coli. Biochem Biophys Res Commun. 2002;292(2):396–401.CrossRefPubMed
26.
go back to reference Phan MD, et al. The serum resistome of a globally disseminated multidrug resistant uropathogenic Escherichia coli clone. PLoS Genet. 2013;9(10):e1003834.CrossRefPubMedPubMedCentral Phan MD, et al. The serum resistome of a globally disseminated multidrug resistant uropathogenic Escherichia coli clone. PLoS Genet. 2013;9(10):e1003834.CrossRefPubMedPubMedCentral
27.
go back to reference Weiser JN, Gotschlich EC. Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect Immun. 1991;59(7):2252–8.PubMedPubMedCentral Weiser JN, Gotschlich EC. Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect Immun. 1991;59(7):2252–8.PubMedPubMedCentral
28.
go back to reference Rupp ME, Fey PD. Extended spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs. 2003;63(4):353–65.CrossRefPubMed Rupp ME, Fey PD. Extended spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs. 2003;63(4):353–65.CrossRefPubMed
29.
go back to reference Ranjan A, et al. Molecular epidemiology and genome dynamics of New Delhi metallo-beta-lactamase (NDM) producing extraintestinal pathogenic E. coli (ExPEC) strains from India. Antimicrob Agents Chemother. 2016;60:6795–805.CrossRefPubMedPubMedCentral Ranjan A, et al. Molecular epidemiology and genome dynamics of New Delhi metallo-beta-lactamase (NDM) producing extraintestinal pathogenic E. coli (ExPEC) strains from India. Antimicrob Agents Chemother. 2016;60:6795–805.CrossRefPubMedPubMedCentral
30.
go back to reference Ubeda C, Djukovic A, Isaac S. Roles of the intestinal microbiota in pathogen protection. Clin Transl Immunol. 2017;6(2):e128.CrossRef Ubeda C, Djukovic A, Isaac S. Roles of the intestinal microbiota in pathogen protection. Clin Transl Immunol. 2017;6(2):e128.CrossRef
31.
go back to reference Sukupolvi S, et al. Plasmid-mediated serum resistance in Salmonella enterica. Microb Pathog. 1992;12(3):219–25.CrossRefPubMed Sukupolvi S, et al. Plasmid-mediated serum resistance in Salmonella enterica. Microb Pathog. 1992;12(3):219–25.CrossRefPubMed
32.
go back to reference Leying H, et al. The capsular polysaccharide is a major determinant of serum resistance in K-1-positive blood culture isolates of Escherichia coli. Infect Immun. 1990;58(1):222–7.PubMedPubMedCentral Leying H, et al. The capsular polysaccharide is a major determinant of serum resistance in K-1-positive blood culture isolates of Escherichia coli. Infect Immun. 1990;58(1):222–7.PubMedPubMedCentral
33.
go back to reference Hussain A, et al. Multiresistant uropathogenic Escherichia coli from a region in India where urinary tract infections are endemic: genotypic and phenotypic characteristics of sequence type 131 isolates of the CTX-M-15 extended-spectrum-beta-lactamase-producing lineage. Antimicrob Agents Chemother. 2012;56(12):6358–65.CrossRefPubMedPubMedCentral Hussain A, et al. Multiresistant uropathogenic Escherichia coli from a region in India where urinary tract infections are endemic: genotypic and phenotypic characteristics of sequence type 131 isolates of the CTX-M-15 extended-spectrum-beta-lactamase-producing lineage. Antimicrob Agents Chemother. 2012;56(12):6358–65.CrossRefPubMedPubMedCentral
34.
go back to reference Sahly H, et al. Increased serum resistance in Klebsiella pneumoniae strains producing extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 2004;48(9):3477–82.CrossRefPubMedPubMedCentral Sahly H, et al. Increased serum resistance in Klebsiella pneumoniae strains producing extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 2004;48(9):3477–82.CrossRefPubMedPubMedCentral
Metadata
Title
ESBL-plasmid carriage in E. coli enhances in vitro bacterial competition fitness and serum resistance in some strains of pandemic sequence types without overall fitness cost
Authors
Amit Ranjan
Julia Scholz
Torsten Semmler
Lothar H. Wieler
Christa Ewers
Stefanie Müller
Derek J. Pickard
Peter Schierack
Karsten Tedin
Niyaz Ahmed
Katharina Schaufler
Sebastian Guenther
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2018
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-018-0243-z

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