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Applied and Environmental Microbiology, April 2008, p. 2187-2199, Vol. 74, No. 7
0099-2240/08/$08.00+0     doi:10.1128/AEM.01214-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Packaging of Live Legionella pneumophila into Pellets Expelled by Tetrahymena spp. Does Not Require Bacterial Replication and Depends on a Dot/Icm-Mediated Survival Mechanism{triangledown}

Sharon G. Berk,1 Gary Faulkner,2 Elizabeth Garduño,2 Mark C. Joy,1 Marco A. Ortiz-Jimenez,3 and Rafael A. Garduño2,4*

Center for the Management, Utilization and Protection of Water Resources, Tennessee Technological University, Cookeville, Tennessee,1 Department of Microbiology and Immunology, Dalhousie University, Halifax, Nova Scotia, Canada,2 Instituto de Investigaciones Biomédicas, Universidad Autónoma de México, Mexico City, D.F., Mexico,3 Department of Medicine-Division of Infectious Diseases, Dalhousie University, Halifax, Nova Scotia, Canada4

Received 31 May 2007/ Accepted 25 January 2008

The freshwater ciliate Tetrahymena sp. efficiently ingested, but poorly digested, virulent strains of the gram-negative intracellular pathogen Legionella pneumophila. Ciliates expelled live legionellae packaged in free spherical pellets. The ingested legionellae showed no ultrastructural indicators of cell division either within intracellular food vacuoles or in the expelled pellets, while the number of CFU consistently decreased as a function of time postinoculation, suggesting a lack of L. pneumophila replication inside Tetrahymena. Pulse-chase feeding experiments with fluorescent L. pneumophila and Escherichia coli indicated that actively feeding ciliates maintain a rapid and steady turnover of food vacuoles, so that the intravacuolar residence of the ingested bacteria was as short as 1 to 2 h. L. pneumophila mutants with a defective Dot/Icm virulence system were efficiently digested by Tetrahymena sp. In contrast to pellets of virulent L. pneumophila, the pellets produced by ciliates feeding on dot mutants contained very few bacterial cells but abundant membrane whorls. The whorls became labeled with a specific antibody against L. pneumophila OmpS, indicating that they were outer membrane remnants of digested legionellae. Ciliates that fed on genetically complemented dot mutants produced numerous pellets containing live legionellae, establishing the importance of the Dot/Icm system to resist digestion. We thus concluded that production of pellets containing live virulent L. pneumophila depends on bacterial survival (mediated by the Dot/Icm system) and occurs in the absence of bacterial replication. Pellets of virulent L. pneumophila may contribute to the transmission of Legionnaires’ disease, an issue currently under investigation.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Dalhousie University, Sir Charles Tupper Building, 7th floor, 5850 College Street, Halifax, Nova Scotia B3H-1X5, Canada. Phone: (902) 494-6575. Fax: (902) 494-5125. E-mail: rafael.garduno{at}dal.ca

{triangledown} Published ahead of print on 1 February 2008.

Applied and Environmental Microbiology, April 2008, p. 2187-2199, Vol. 74, No. 7
0099-2240/08/$08.00+0     doi:10.1128/AEM.01214-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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  • Faulkner, G., Berk, S. G., Garduno, E., Ortiz-Jimenez, M. A., Garduno, R. A. (2008). Passage through Tetrahymena tropicalis Triggers a Rapid Morphological Differentiation in Legionella pneumophila. J. Bacteriol. 190: 7728-7738 [Abstract] [Full Text]  


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