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Journal of Bacteriology, May 2002, p. 2352-2359, Vol. 184, No. 9
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.9.2352-2359.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Population Heterogeneity of Salmonella enterica Serotype Typhimurium Resulting from Phase Variation of the lpf Operon In Vitro and In Vivo

Robert A. Kingsley, Eric H. Weening, A. Marijke Keestra, and Andreas J. Bäumler*

Department of Medical Microbiology and Immunology, College of Medicine, Texas A&M University System Health Science Center, College Station, Texas 77843-1114

Received 17 December 2001/ Accepted 5 February 2002

The lpf fimbrial operon oscillates between phase ON and phase OFF expression states, thereby generating heterogeneity within S. enterica serotype Typhimurium populations with regard to expression of long polar fimbrial antigens. To determine whether the proportion of lpf phase variants changes with growth conditions, the lpf phase ON content of cultures was determined after in vitro and in vivo passage. After passage in Luria-Bertani (LB) broth for 120 generations, 96% of cells in a serotype Typhimurium culture carried the lpf operon in the phase ON expression state, regardless of the phase ON/OFF ratio in the inoculum. In contrast, a culture passaged on LB agar plates for 500 generations contained approximately 2% lpf phase ON cells. Differences in the lpf phase ON content of cultures passaged in broth and on plates were not caused by an outgrowth of lpf phase ON or lpf phase OFF cells, since deletion of lpf biosynthesis genes did not alter the phase ON/OFF ratio attained after passage. Instead, growth in LB broth resulted in a eightfold increase in the phase OFF-to-ON transition frequency and a decrease of the lpf phase ON-to-OFF transition frequency by a factor of 150 compared to growth on LB agar plates. After infection of naïve CBA/J mice with an lpf phase ON culture of serotype Typhimurium, the proportion of lpf phase ON cells continuously decreased over time, regardless of whether the strain carried intact fimbrial biosynthesis genes. These data suggest that elaboration of fimbriae does not have a major influence on the population heterogeneity produced by phase variation of the lpf operon in naïve mice.

* Corresponding author. Mailing address: Department of Medical Microbiology and Immunology, College of Medicine, Texas A&M University System Health Science Center, Reynolds Medical Building, College Station, TX 77843-1114. Phone: (979) 862-7756. Fax: (979) 845-3479. E-mail: abaumler{at}tamu.edu.

Journal of Bacteriology, May 2002, p. 2352-2359, Vol. 184, No. 9
0021-9193/02/$04.00+0     DOI: 10.1128/JB.184.9.2352-2359.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Ledeboer, N. A., Frye, J. G., McClelland, M., Jones, B. D. (2006). Salmonella enterica Serovar Typhimurium Requires the Lpf, Pef, and Tafi Fimbriae for Biofilm Formation on HEp-2 Tissue Culture Cells and Chicken Intestinal Epithelium.. Infect. Immun. 74: 3156-3169 [Abstract] [Full Text]  
  • Weening, E. H., Barker, J. D., Laarakker, M. C., Humphries, A. D., Tsolis, R. M., Baumler, A. J. (2005). The Salmonella enterica Serotype Typhimurium lpf, bcf, stb, stc, std, and sth Fimbrial Operons Are Required for Intestinal Persistence in Mice. Infect. Immun. 73: 3358-3366 [Abstract] [Full Text]  


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