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Journal of Bacteriology, November 2005, p. 7716-7726, Vol. 187, No. 22
0021-9193/05/$08.00+0     doi:10.1128/JB.187.22.7716-7726.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Evidence for Acquisition of Legionella Type IV Secretion Substrates via Interdomain Horizontal Gene Transfer

Karim Suwwan de Felipe,1,2 Sergey Pampou,2,3 Oliver S. Jovanovic,2 Christopher D. Pericone,2 Senna F. Ye,2 Sergey Kalachikov,3 and Howard A. Shuman1,2*

Integrated Program in Cellular, Molecular & Biophysical Studies,1 Department of Microbiology,2 Columbia Genome Center, Columbia University Medical Center, 701 West 168th Street, New York, New York 100323

Received 16 May 2005/ Accepted 24 August 2005

Intracellular pathogens exploit host cell functions to create a replication niche inside eukaryotic cells. The causative agent of Legionnaires' disease, the {gamma}-proteobacterium Legionella pneumophila, resides and replicates within a modified vacuole of protozoan and mammalian cells. L. pneumophila translocates effector proteins into host cells through the Icm-Dot complex, a specialized type IVB secretion system that is required for intracellular growth. To find out if some effector proteins may have been acquired through interdomain horizontal gene transfer (HGT), we performed a bioinformatic screen that searched for eukaryotic motifs in all open reading frames of the L. pneumophila Philadelphia-1 genome. We found 44 uncharacterized genes with many distinct eukaryotic motifs. Most of these genes contain G+C biases compared to other L. pneumophila genes, supporting the theory that they were acquired through HGT. Furthermore, we found that several of them are expressed and up-regulated in stationary phase in an RpoS-dependent manner. In addition, at least seven of these gene products are translocated into host cells via the Icm-Dot complex, confirming their role in the intracellular environment. Reminiscent of the case with most Icm-Dot substrates, most of the strains containing mutations in these genes grew comparably to the parent strain intracellularly. Our findings suggest that in L. pneumophila, interdomain HGT may have been a major mechanism for the acquisition of determinants of infection.

* Corresponding author. Mailing address: Department of Microbiology, Columbia University Medical Center, 701 West 168th Street, New York, New York 10032. Phone: (212) 305-6913. Fax: (212) 305-1468. E-mail: has7{at}columbia.edu.

Journal of Bacteriology, November 2005, p. 7716-7726, Vol. 187, No. 22
0021-9193/05/$08.00+0     doi:10.1128/JB.187.22.7716-7726.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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