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Infection and Immunity, January 2007, p. 358-370, Vol. 75, No. 1
0019-9567/07/$08.00+0     doi:10.1128/IAI.00716-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

The YfgL Lipoprotein Is Essential for Type III Secretion System Expression and Virulence of Salmonella enterica Serovar Enteritidis{triangledown} ,{dagger}

Yann Fardini,1,{ddagger} Kamel Chettab,1,{ddagger} Olivier Grépinet,1 Sandrine Rochereau,1 Jérôme Trotereau,1 Philippa Harvey,2 Maïté Amy,1 Elisabeth Bottreau,1 Nat Bumstead,2 Paul A. Barrow,2,§ and Isabelle Virlogeux-Payant1*

Institut National de la Recherche Agronomique, Centre de Tours-Nouzilly, Infectiologie Animale et Santé Publique, 37380 Nouzilly, France,1 Institute for Animal Health, Compton Laboratory, Division of Environmental Microbiology Newbury, Berkshire RG20 7NN, United Kingdom2

Received 4 May 2006/ Returned for modification 26 July 2006/ Accepted 11 October 2006

Salmonella enterica, like many gram-negative pathogens, uses type three secretion systems (TTSS) to infect its hosts. The three TTSS of Salmonella, namely, TTSS-1, TTSS-2, and flagella, play a major role in the virulence of this bacterium, allowing it to cross the intestinal barrier and to disseminate systemically. Previous data from our laboratory have demonstrated the involvement of the chromosomal region harboring the yfgL, engA, and yfgJ open reading frames in S. enterica serovar Enteritidis virulence. Using microarray analysis and real-time reverse transcription-PCR after growth of bacterial cultures favorable for either TTSS-1 or TTSS-2 expression, we show in this study that the deletion in S. enterica serovar Enteritidis of yfgL, encoding an outer membrane lipoprotein, led to the transcriptional down-regulation of most Salmonella pathogenicity island 1 (SPI-1), SPI-2, and flagellar genes encoding the TTSS structural proteins and effector proteins secreted by these TTSS. In line with these results, the virulence of the {Delta}yfgL mutant was greatly attenuated in mice. Moreover, even if YfgL is involved in the assembly of outer membrane proteins, the regulation of TTSS expression observed was not due to an inability of the {Delta}yfgL mutant to assemble TTSS in its membrane. Indeed, when we forced the transcription of SPI-1 genes by constitutively expressing HilA, the secretion of the TTSS-1 effector protein SipA was restored in the culture supernatant of the mutant. These results highlight the crucial role of the outer membrane lipoprotein YfgL in the expression of all Salmonella TTSS and, thus, in the virulence of Salmonella. Therefore, this outer membrane protein seems to be a privileged target for fighting Salmonella.

* Corresponding author. Mailing address: Institut National de la Recherche Agronomique, Centre de Tours-Nouzilly, Laboratoire Infectiologie Animale et Santé Publique, Bâtiment 311, 37380 Nouzilly, France. Phone: 33 (0)2 47 42 76 60. Fax: 33 (0)2 47 42 77 79. E-mail: Isabelle.Virlogeux{at}tours.inra.fr.

{triangledown} Published ahead of print on 23 October 2006.

Editor: V. J. DiRita

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

{ddagger} Y.F. and K.C. contributed equally to this work.

§ Present address: School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Loughborough, Leicestershire LE12 5RD, United Kingdom.

Infection and Immunity, January 2007, p. 358-370, Vol. 75, No. 1
0019-9567/07/$08.00+0     doi:10.1128/IAI.00716-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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