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Infection and Immunity, May 2008, p. 1825-1836, Vol. 76, No. 5
0019-9567/08/$08.00+0     doi:10.1128/IAI.01396-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Proteomic Characterization of the Whole Secretome of Legionella pneumophila and Functional Analysis of Outer Membrane Vesicles{triangledown} ,{dagger}

Frank Galka,1 Sun Nyunt Wai,2 Harald Kusch,3 Susanne Engelmann,3 Michael Hecker,3 Bernd Schmeck,4 Stefan Hippenstiel,4 Bernt Eric Uhlin,2 and Michael Steinert5*

Institut für Molekulare Infektionsbiologie, Julius-Maximilians-Universität Würzburg, Röntgenring 11, D-97070 Würzburg, Germany,1 Department of Molecular Biology, Umeå University, S-901 87 Umeå, Sweden,2 Institut für Mikrobiologie, Ernst-Moritz-Arndt-Universität, F.-L.-Jahn-Str. 15, D-17487 Greifswald, Germany,3 Medizinische Klinik m. S. Infektiologie und Pneumologie, Charité, Universitätsmedizin Berlin, Augustenburger Platz 1, D-13353 Berlin, Germany,4 Institut für Mikrobiologie, Technische Universität Braunschweig, Spielmannstr. 7, D-38106 Braunschweig, Germany5

Received 17 October 2007/ Returned for modification 27 November 2007/ Accepted 27 January 2008

Secretion of effector molecules is one of the major mechanisms by which the intracellular human pathogen Legionella pneumophila interacts with host cells during infection. Specific secretion machineries which are responsible for the subfraction of secreted proteins (soluble supernatant proteins [SSPs]) and the production of bacterial outer membrane vesicles (OMVs) both contribute to the protein composition of the extracellular milieu of this lung pathogen. Here we present comprehensive proteome reference maps for both SSPs and OMVs. Protein identification and assignment analyses revealed a total of 181 supernatant proteins, 107 of which were specific to the SSP fraction and 33 of which were specific to OMVs. A functional classification showed that a large proportion of the identified OMV proteins are involved in the pathogenesis of Legionnaires' disease. Zymography and enzyme assays demonstrated that the SSP and OMV fractions possess proteolytic and lipolytic enzyme activities which may contribute to the destruction of the alveolar lining during infection. Furthermore, it was shown that OMVs do not kill host cells but specifically modulate their cytokine response. Binding of immunofluorescently stained OMVs to alveolar epithelial cells, as visualized by confocal laser scanning microscopy, suggested that there is delivery of a large and complex group of proteins and lipids in the infected tissue in association with OMVs. On the basis of these new findings, we discuss the relevance of protein sorting and compartmentalization of virulence factors, as well as environmental aspects of the vesicle-mediated secretion.

* Corresponding author. Mailing address: Institut für Mikrobiologie, Technische Universität Braunschweig, Spielmannstr. 7, D-38106 Braunschweig, Germany. Phone: (49) 531 3915802. Fax: (49) 531 3915854. E-mail: m.steinert{at}tu-bs.de

{triangledown} Published ahead of print on 4 February 2008.

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

Editor: A. Camilli

Infection and Immunity, May 2008, p. 1825-1836, Vol. 76, No. 5
0019-9567/08/$08.00+0     doi:10.1128/IAI.01396-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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