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Applied and Environmental Microbiology, August 2009, p. 5179-5185, Vol. 75, No. 16
0099-2240/09/$08.00+0     doi:10.1128/AEM.00334-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Respective Roles of Culturable and Viable-but-Nonculturable Cells in the Heterogeneity of Salmonella enterica Serovar Typhimurium Invasiveness{triangledown}

Julien Passerat,1,{dagger} Patrice Got,1 Sam Dukan,2 and Patrick Monfort1*

Laboratoire Écosystèmes Lagunaires, UMR 5119 CNRS, Université Montpellier II, Place Eugène Bataillon, 34095 Montpellier, France,1 Laboratoire de Chimie Bactérienne, Université Aix Marseille, IFR88, UPR 9043 CNRS, 31 Chemin Joseph Aiguier, 13402 Marseille, France2

Received 10 February 2009/ Accepted 3 June 2009

The existence of Salmonella enterica serovar Typhimurium viable-but-nonculturable (VBNC) cells is a public health concern since they could constitute unrecognized sources of infection if they retain their pathogenicity. To date, many studies have addressed the ability of S. Typhimurium VBNC cells to remain infectious, but their conclusions are conflicting. An assumption could explain these conflicting results. It has been proposed that infectivity could be retained only temporarily after entry into the VBNC state and that most VBNC cells generated under intense stress could exceed the stage where they are still infectious. Using a Radioselectan density gradient centrifugation technique makes it possible to increase the VBNC-cell/culturable-cell ratio without increasing the exposure to stress and, consequently, to work with a larger proportion of newly VBNC cells. Here, we observed that (i) in the stationary phase, the S. Typhimurium population comprised three distinct subpopulations at 10, 24, or 48 h of culture; (ii) the VBNC cells were detected at 24 and 48 h; (iii) measurement of invasion gene (hilA, invF, and orgA) expression demonstrated that cells are highly heterogeneous within a culturable population; and (iv) invasion assays of HeLa cells showed that culturable cells from the different subpopulations do not display the same invasiveness. The results also suggest that newly formed VBNC cells are either weakly able or not able to successfully initiate epithelial cell invasion. Finally, we propose that at entry into the stationary phase, invasiveness may be one way for populations of S. Typhimurium to escape stochastic alteration leading to cell death.

* Corresponding author. Mailing address: Laboratoire Écosystèmes Lagunaires, UMR 5119 CNRS, Université Montpellier II, Place Eugène Bataillon, 34095 Montpellier, France. Phone: 33 (0)4 67 14 48 22. Fax: 33 (0)4 67 14 37 19. E-mail: pmonfort{at}univ-montp2.fr

{triangledown} Published ahead of print on 12 June 2009.

{dagger} Present address: Écologie des Systèmes Aquatiques, Université Libre de Bruxelles, CP221 Boulevard du Triomphe, B-1050 Brussels, Belgium.

Applied and Environmental Microbiology, August 2009, p. 5179-5185, Vol. 75, No. 16
0099-2240/09/$08.00+0     doi:10.1128/AEM.00334-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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