In Vivo Transmission of an IncA/C Plasmid in Escherichia coli Depends on Tetracycline Concentration, and Acquisition of the Plasmid Results in a Variable Cost of Fitness - PubMed (original) (raw)

. 2015 May 15;81(10):3561-70.

doi: 10.1128/AEM.04193-14. Epub 2015 Mar 13.

Randall S Singer 2, Richard E Isaacson 2, Jessica L Danzeisen 2, Kevin Lang 2, Kristi Kobluk 2, Bernadette Rivet 2, Klaudyna Borewicz 2, Jonathan G Frye 3, Mark Englen 3, Janet Anderson 2, Peter R Davies 4

Affiliations

In Vivo Transmission of an IncA/C Plasmid in Escherichia coli Depends on Tetracycline Concentration, and Acquisition of the Plasmid Results in a Variable Cost of Fitness

Timothy J Johnson et al. Appl Environ Microbiol. 2015.

Abstract

IncA/C plasmids are broad-host-range plasmids enabling multidrug resistance that have emerged worldwide among bacterial pathogens of humans and animals. Although antibiotic usage is suspected to be a driving force in the emergence of such strains, few studies have examined the impact of different types of antibiotic administration on the selection of plasmid-containing multidrug resistant isolates. In this study, chlortetracycline treatment at different concentrations in pig feed was examined for its impact on selection and dissemination of an IncA/C plasmid introduced orally via a commensal Escherichia coli host. Continuous low-dose administration of chlortetracycline at 50 g per ton had no observable impact on the proportions of IncA/C plasmid-containing E. coli from pig feces over the course of 35 days. In contrast, high-dose administration of chlortetracycline at 350 g per ton significantly increased IncA/C plasmid-containing E. coli in pig feces (P < 0.001) and increased movement of the IncA/C plasmid to other indigenous E. coli hosts. There was no evidence of conjugal transfer of the IncA/C plasmid to bacterial species other than E. coli. In vitro competition assays demonstrated that bacterial host background substantially impacted the cost of IncA/C plasmid carriage in E. coli and Salmonella. In vitro transfer and selection experiments demonstrated that tetracycline at 32 μg/ml was necessary to enhance IncA/C plasmid conjugative transfer, while subinhibitory concentrations of tetracycline in vitro strongly selected for IncA/C plasmid-containing E. coli. Together, these experiments improve our knowledge on the impact of differing concentrations of tetracycline on the selection of IncA/C-type plasmids.

Copyright © 2015, American Society for Microbiology. All Rights Reserved.

PubMed Disclaimer

Figures

FIG 1

FIG 1

Enumeration of total and IncA/C plasmid-containing E. coli in pig feces over 35 days postinoculation. The y axis represents the CFU per gram of feces. Days represent sampling days postinoculation with IncA/C plasmid-containing E. coli. Light gray bars indicate total E. coli counts, and dark gray bars indicate IncA/C plasmid-containing E. coli counts. “Control (−)” indicates an noninoculated control, and “Control (+)” indicates an IncA/C+ E. coli-inoculated control without antibiotic treatment.

FIG 2

FIG 2

Enumeration of total and tetracycline-resistant E. coli in pig feces at selected time points. See the Fig. 1 legend for a description.

FIG 3

FIG 3

Relative fitness cost of IncA/C plasmid carriage on various Salmonella and E. coli recipients. A positive value indicates a cost for plasmid carriage, whereas a negative value indicates a benefit for plasmid carriage. Serotype or phylogenetic group is displayed below each bar. Error is expressed as the standard error of the mean. Each bar represents multiple isolates examined.

FIG 4

FIG 4

Relative fitness cost of plasmid combinations in various E. coli hosts. A positive value indicates a cost for plasmid carriage, whereas a negative value indicates a benefit for plasmid carriage. Multiple isolates from each phylogenetic group were examined for cost of carriage of an IncA/C plasmid alone (pAC), an IncI1 plasmid alone (pI1), or cocarriage of both plasmids (pACpI1).

FIG 5

FIG 5

Frequency of conjugal transfer in the presence of increasing concentrations of tetracycline, presented as transconjugants/donor (y axis).

FIG 6

FIG 6

Competition experiments between pAR060302-containing and pAR060302-lacking E. coli K-12 in the presence of increasing subinhibitory concentrations of tetracycline. The y axis depicts the percentage of pAR060302-containing colonies recovered relative to plasmid lacking colonies. Time zero represents the starting material for all concentrations mixed at equal doses, which was then quantified via direct plating.

Similar articles

Cited by

References

    1. McIntosh D, Cunningham M, Ji B, Fekete FA, Parry EM, Clark SE, Zalinger ZB, Gilg IC, Danner GR, Johnson KA, Beattie M, Ritchie R. 2008. Transferable, multiple antibiotic and mercury resistance in Atlantic Canadian isolates of Aeromonas salmonicida subsp. salmonicida is associated with carriage of an IncA/C plasmid similar to the Salmonella enterica plasmid pSN254. J Antimicrob Chemother 61:1221–1228. doi:10.1093/jac/dkn123. - DOI - PMC - PubMed
    1. Verner-Jeffreys DW, Welch TJ, Schwarz T, Pond MJ, Woodward MJ, Haig SJ, Rimmer GS, Roberts E, Morrison V, Baker-Austin C. 2009. High prevalence of multidrug-tolerant bacteria and associated antimicrobial resistance genes isolated from ornamental fish and their carriage water. PLoS One 4:e8388. doi:10.1371/journal.pone.0008388. - DOI - PMC - PubMed
    1. Daniels JB, Call DR, Besser TE. 2007. Molecular epidemiology of blaCMY-2 plasmids carried by Salmonella enterica and Escherichia coli isolates from cattle in the Pacific Northwest. Appl Environ Microbiol 73:8005–8011. doi:10.1128/AEM.01325-07. - DOI - PMC - PubMed
    1. Frye JG, Fedorka-Cray PJ. 2007. Prevalence, distribution and characterisation of ceftiofur resistance in Salmonella enterica isolated from animals in the USA from 1999 to 2003. Int J Antimicrob Agents 30:134–142. doi:10.1016/j.ijantimicag.2007.03.013. - DOI - PubMed
    1. Zhao S, White DG, McDermott PF, Friedman S, English L, Ayers S, Meng J, Maurer JJ, Holland R, Walker RD. 2001. Identification and expression of cephamycinase blaCMY genes in Escherichia coli and Salmonella isolates from food animals and ground meat. Antimicrob Agents Chemother 45:3647–3650. doi:10.1128/AAC.45.12.3647-3650.2001. - DOI - PMC - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources