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Journal of Bacteriology, October 2008, p. 6779-6794, Vol. 190, No. 20
0021-9193/08/$08.00+0     doi:10.1128/JB.00661-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Insights into the Environmental Resistance Gene Pool from the Genome Sequence of the Multidrug-Resistant Environmental Isolate Escherichia coli SMS-3-5 ^,

W. Florian Fricke,¹ Meredith S. Wright,^2, Angela H. Lindell,² Derek M. Harkins,³ Craig Baker-Austin,^2, Jacques Ravel,^1* and Ramunas Stepanauskas⁴

Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland 21201,¹ Savannah River Ecology Laboratory, University of Georgia, Aiken, South Carolina 29802,² The J. Craig Venter Institute, Rockville, Maryland 20850,³ Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, Maine 04575⁴

Received 12 May 2008/ Accepted 2 August 2008

The increasing occurrence of multidrug-resistant pathogens of clinical and agricultural importance is a global public health concern. While antimicrobial use in human and veterinary medicine is known to contribute to the dissemination of antimicrobial resistance, the impact of microbial communities and mobile resistance genes from the environment in this process is not well understood. Isolated from an industrially polluted aquatic environment, Escherichia coli SMS-3-5 is resistant to a record number of antimicrobial compounds from all major classes, including two front-line fluoroquinolones (ciprofloxacin and moxifloxacin), and in many cases at record-high concentrations. To gain insights into antimicrobial resistance in environmental bacterial populations, the genome of E. coli SMS-3-5 was sequenced and compared to the genome sequences of other E. coli strains. In addition, selected genetic loci from E. coli SMS-3-5 predicted to be involved in antimicrobial resistance were phenotypically characterized. Using recombinant vector clones from shotgun sequencing libraries, resistance to tetracycline, streptomycin, and sulfonamide/trimethoprim was assigned to a single mosaic region on a 130-kb plasmid (pSMS35_130). The remaining plasmid backbone showed similarity to virulence plasmids from avian-pathogenic E. coli (APEC) strains. Individual resistance gene cassettes from pSMS35_130 are conserved among resistant bacterial isolates from multiple phylogenetic and geographic sources. Resistance to quinolones was assigned to several chromosomal loci, mostly encoding transport systems that are also present in susceptible E. coli isolates. Antimicrobial resistance in E. coli SMS-3-5 is therefore dependent both on determinants acquired from a mobile gene pool that is likely available to clinical and agricultural pathogens, as well, and on specifically adapted multidrug efflux systems. The association of antimicrobial resistance with APEC virulence genes on pSMS35_130 highlights the risk of promoting the spread of virulence through the extensive use of antibiotics.

Published ahead of print on 15 August 2008.

Supplemental material for this article may be found at http://jb.asm.org/.

Present address: Flathead Lake Biological Station, University of Montana, Polson, MT 59860.

Present address: Centre for Environment Fisheries and Aquaculture Science, Weymouth, Dorset DT4 8UB, United Kingdom.