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Applied and Environmental Microbiology, November 2003, p. 6669-6675, Vol. 69, No. 11
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.11.6669-6675.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Induction and Resuscitation of Viable but Nonculturable Salmonella enterica Serovar Typhimurium DT104{dagger}

A. R. Gupte, C. L. E. de Rezende, and S. W. Joseph*

Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742

Received 16 May 2003/ Accepted 28 August 2003

Salmonella enterica serovar Typhimurium DT104 11601was tested for its ability to maintain viability in minimal, chemically defined solutions. Periodic monitoring of growth and survival in microcosms of different ion concentrations, maintained at various temperatures, showed a gradual decline in culturable organisms (~235 days) at 5°C. Organisms maintained at a higher temperature (21°C) showed continuous, equivalent CFU per milliliter (~106) up to 400 days after inoculation. Fluorescence microscopy with Baclight revealed that nonculturable cells were actually viable, while observations with scanning electron microscopy showed that the cells had retained their structural integrity. Temperature upshift (56°C ± 0.5, 15 s) of the nonculturable organisms (5°C) in Trypticase soy broth followed by immediate inoculation onto Trypticase soy agar (TSA) gave evidence of resuscitation. Interestingly, S. enterica serovar Typhimurium DT104 from the microcosms at either 5°C (1 to 200 days) or 21°C (1 to 250 days) did not show enhanced growth after intermittent inoculation onto catalase-supplemented TSA. Furthermore, cells from 21°C microcosms exposed to oxidative and osmotic stress showed greater resistance to stresses over increasing times of exposure than did recently grown cells. It is possible that the exceptional survivability and resilience of this particular strain may in part reflect the growing importance of this multidrug-resistant organism, in general, as a cause of intestinal disease in humans. The fact that S. enterica serovar Typhimurium DT104 11601 is capable of modifying its physiological characteristics, including entry into and recovery from the viable but nonculturable state, suggests the overall possibility that S. enterica serovar Typhimurium DT104 may be able to respond uniquely to various adverse environmental conditions.

* Corresponding author. Mailing address: Department of Cell Biology and Molecular Genetics, Microbiology Building, University of Maryland, College Park, MD 20742. Phone: (301) 405-5452. Fax: (301) 314-9489. E-mail: sj13{at}umail.umd.edu.

{dagger} The electron microscopy work described herein is contribution no. 98 from the Laboratory of Biological Ultrastructure at the University of Maryland, College Park.

Applied and Environmental Microbiology, November 2003, p. 6669-6675, Vol. 69, No. 11
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.11.6669-6675.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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