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Applied and Environmental Microbiology, March 2008, p. 1508-1516, Vol. 74, No. 5
0099-2240/08/$08.00+0     doi:10.1128/AEM.01931-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Phenotypic and Proteomic Characterization of Multiply Antibiotic-Resistant Variants of Salmonella enterica Serovar Typhimurium Selected Following Exposure to Disinfectants{triangledown} ,{dagger}

Kimon A. G. Karatzas,1* Luke P. Randall,3 Mark Webber,2 Laura J. V. Piddock,2 Tom J. Humphrey,1 Martin J. Woodward,3 and Nick G. Coldham3

Division of Veterinary Pathology, Infection and Immunity, School of Clinical Veterinary Science, University of Bristol, Langford House, Langford, Bristol BS40 5DU, United Kingdom,1 Antimicrobial Agents Research Group, Division of Immunity and Infection, The Medical School, The University of Birmingham, Birmingham B15 2TT, United Kingdom,2 Department of Food and Environmental Safety, Veterinary Laboratories Agency (Weybridge), New Haw, Addlestone, Surrey KT15 3NB, United Kingdom3

Received 22 August 2007/ Accepted 6 December 2007

In previous work, Salmonella enterica serovar Typhimurium strain SL1344 was exposed to sublethal concentrations of three widely used farm disinfectants in daily serial passages for 7 days in an attempt to investigate possible links between the use of disinfectants and antimicrobial resistance. Stable variants OXCR1, QACFGR2, and TOPR2 were obtained following treatment with an oxidizing compound blend, a quaternary ammonium disinfectant containing formaldehyde and glutaraldehyde, and a tar acid-based disinfectant, respectively. All variants exhibited ca. fourfold-reduced susceptibility to ciprofloxacin, chloramphenicol, tetracycline, and ampicillin. This coincided with reduced levels of outer membrane proteins for all strains and high levels of AcrAB-TolC for OXCR1 and QACFGR2, as demonstrated by two-dimensional high-performance liquid chromatography-mass spectrometry. The protein profiles of OXCR1 and QACFGR2 were similar, but they were different from that of TOPR2. An array of different proteins protecting against oxidants, nitroaromatics, disulfides, and peroxides were overexpressed in all strains. The growth and motility of variants were reduced compared to the growth and motility of the parent strain, the expression of several virulence proteins was altered, and the invasiveness in an enteric epithelial cell line was reduced. The colony morphology of OXCR1 and QACFGR2 was smooth, and both variants exhibited a loss of modal distribution of the lipopolysaccharide O-antigen chain length, favoring the production of short O-antigen chain molecules. Metabolic changes were also detected, suggesting that there was increased protein synthesis and a shift from oxidative phosphorylation to substrate level phosphorylation. In this study, we obtained evidence that farm disinfectants can select for strains with reduced susceptibility to antibiotics, and here we describe changes in protein expression in such strains.

* Corresponding author. Mailing address: Bacterial Stress Response Group, Department of Microbiology, National University of Ireland, Galway, Ireland. Phone: 353 91 495091. Fax: 353 91 494598. E-mail: Kimon-Andreas.Karatzas{at}nuigalway.ie

{triangledown} Published ahead of print on 14 December 2007.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

Applied and Environmental Microbiology, March 2008, p. 1508-1516, Vol. 74, No. 5
0099-2240/08/$08.00+0     doi:10.1128/AEM.01931-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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