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Infection and Immunity, June 2006, p. 3285-3295, Vol. 74, No. 6
0019-9567/06/$08.00+0     doi:10.1128/IAI.01382-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Membrane Vesicles Shed by Legionella pneumophila Inhibit Fusion of Phagosomes with Lysosomes

Esteban Fernandez-Moreira,1 Juergen H. Helbig,2 and Michele S. Swanson1*

Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109-0620,1 Institut Medizinische Mikrobiologie und Hygiene, Medical Faculty TU Dresden, D-01307 Dresden, Germany2

Received 24 August 2005/ Returned for modification 28 October 2005/ Accepted 2 March 2006

When cultured in broth to the transmissive phase, Legionella pneumophila infects macrophages by inhibiting phagosome maturation, whereas replicative-phase cells are transported to the lysosomes. Here we report that the ability of L. pneumophila to inhibit phagosome-lysosome fusion correlated with developmentally regulated modifications of the pathogen's surface, as judged by its lipopolysaccharide profile and by its binding to a sialic acid-specific lectin and to the hydrocarbon hexadecane. Likewise, the composition of membrane vesicles shed by L. pneumophila was developmentally regulated, based on binding to the lectin and to the lipopolysaccharide-specific monoclonal antibody 3/1. Membrane vesicles were sufficient to inhibit phagosome-lysosome fusion by a mechanism independent of type IV secretion, since only ~25% of beads suspended with or coated by vesicles from transmissive phase wild type or dotA secretion mutants colocalized with lysosomal probes, whereas ~75% of beads were lysosomal when untreated or presented with vesicles from the L. pneumophila letA regulatory mutant or E. coli. As observed previously for L. pneumophila infection of mouse macrophages, vesicles inhibited phagosome-lysosome fusion only temporarily; by 10 h after treatment with vesicles, macrophages delivered ~72% of ingested beads to lysosomes. Accordingly, in the context of the epidemiology of the pneumonia Legionnaires' disease and virulence mechanisms of Leishmania and Mycobacteria, we discuss a model here in which L. pneumophila developmentally regulates its surface composition and releases vesicles into phagosomes that inhibit their fusion with lysosomes.

* Corresponding author. Mailing address: University of Michigan Medical School, 6734 Medical Sciences Building II, Ann Arbor, MI 48109-0620. Phone: (734) 647-7295. Fax: (734) 764-3562. E-mail: mswanson{at}umich.edu.

Editor: J. N. Weiser

Infection and Immunity, June 2006, p. 3285-3295, Vol. 74, No. 6
0019-9567/06/$08.00+0     doi:10.1128/IAI.01382-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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