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Applied and Environmental Microbiology, October 2002, p. 4788-4794, Vol. 68, No. 10
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.10.4788-4794.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Resuscitation of Salmonella enterica Serovar Typhimurium and Enterohemorrhagic Escherichia coli from the Viable but Nonculturable State by Heat-Stable Enterobacterial Autoinducer

R. Reissbrodt,1 I. Rienaecker,1 J. M. Romanova,2 P. P. E. Freestone,3 R. D. Haigh,3 M. Lyte,4 H. Tschäpe,1 and P. H. Williams3*

Robert Koch Institute, Wernigerode, Germany,1 Gamaleya Institute, Moscow, Russian Federation,2 Department of Microbiology and Immunology, University of Leicester, Leicester, United Kingdom,3 Minneapolis Medical Research Foundation/Hennepin County Medical Center, Minneapolis, and Minnesota State University at Mankato, Mankato, Minnesota4

Received 15 March 2002/ Accepted 12 July 2002

Salmonella enterica serovar Typhimurium and enterohemorrhagic Escherichia coli were stressed by prolonged incubation in water microcosms until it was no longer possible to observe colony formation when samples were plated on nonselective medium. Overnight incubation of samples in nutrient-rich broth medium supplemented with growth factors, however, allowed resuscitation of stressed and viable but nonculturable cells so that subsequent plating yielded observable colonies for significantly extended periods of time. The growth factors were (i) the trihydroxamate siderophore ferrioxamine E (for Salmonella only), (ii) the commercially available antioxidant Oxyrase, and (iii) the heat-stable autoinducer of growth secreted by enterobacterial species in response to norepinephrine. Analysis of water microcosms with the Bioscreen C apparatus confirmed that these supplements enhanced recovery of cells in stressed populations; enterobacterial autoinducer was the most effective, promoting resuscitation in populations that were so heavily stressed that ferrioxamine E or Oxyrase had no effect. Similar results were observed in Bioscreen analysis of bacterial populations stressed by heating. Patterns of resuscitation of S. enterica serovar Typhimurium rpoS mutants from water microcosms and heat stress were qualitatively similar, suggesting that the general stress response controlled by the {sigma}s subunit of RNA polymerase plays no role in autoinducer-dependent resuscitation. Enterobacterial autoinducer also resuscitated stressed populations of Citrobacter freundii and Enterobacter agglomerans.

* Corresponding author. Mailing address: University of Leicester, Department of Microbiology and Immunology, Maurice Shock Medical Sciences Building, University Rd., Leicester LE1 9HN, United Kingdom. Phone: (44)-116-252-3436. Fax: (44)-116-252-5030. E-mail: phw2{at}le.ac.uk.

Applied and Environmental Microbiology, October 2002, p. 4788-4794, Vol. 68, No. 10
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.10.4788-4794.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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