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Journal of Bacteriology, April 2009, p. 2461-2473, Vol. 191, No. 8
0021-9193/09/$08.00+0     doi:10.1128/JB.01578-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

{sigma}S Controls Multiple Pathways Associated with Intracellular Multiplication of Legionella pneumophila{triangledown} ,{dagger}

Galadriel Hovel-Miner,1 Sergey Pampou,2 Sebastien P. Faucher,1 Margaret Clarke,3 Irina Morozova,2 Pavel Morozov,2 James J. Russo,2 Howard A. Shuman,1* and Sergey Kalachikov2

Department of Microbiology, Columbia University Medical Center, 701 West 168th Street, New York, New York 10032,1 Columbia Genome Center, Columbia University Medical Center, 1150 St. Nicholas Avenue, New York, New York 10032,2 Oklahoma Medical Research Foundation, Program in Genetic Models of Disease, 825 Northeast 13th Street, Oklahoma City, Oklahoma 731043

Received 6 November 2008/ Accepted 4 February 2009

Legionella pneumophila is the causative agent of the severe and potentially fatal pneumonia Legionnaires' disease. L. pneumophila is able to replicate within macrophages and protozoa by establishing a replicative compartment in a process that requires the Icm/Dot type IVB secretion system. The signals and regulatory pathways required for Legionella infection and intracellular replication are poorly understood. Mutation of the rpoS gene, which encodes {sigma}S, does not affect growth in rich medium but severely decreases L. pneumophila intracellular multiplication within protozoan hosts. To gain insight into the intracellular multiplication defect of an rpoS mutant, we examined its pattern of gene expression during exponential and postexponential growth. We found that {sigma}S affects distinct groups of genes that contribute to Legionella intracellular multiplication. We demonstrate that rpoS mutants have a functional Icm/Dot system yet are defective for the expression of many genes encoding Icm/Dot-translocated substrates. We also show that {sigma}S affects the transcription of the cpxR and pmrA genes, which encode two-component response regulators that directly affect the transcription of Icm/Dot substrates. Our characterization of the L. pneumophila small RNA csrB homologs, rsmY and rsmZ, introduces a link between {sigma}S and the posttranscriptional regulator CsrA. We analyzed the network of {sigma}S-controlled genes by mutational analysis of transcriptional regulators affected by {sigma}S. One of these, encoding the L. pneumophila arginine repressor homolog gene, argR, is required for maximal intracellular growth in amoebae. These data show that {sigma}S is a key regulator of multiple pathways required for L. pneumophila intracellular multiplication.

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

{triangledown} Published ahead of print on 13 February 2009.

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

Journal of Bacteriology, April 2009, p. 2461-2473, Vol. 191, No. 8
0021-9193/09/$08.00+0     doi:10.1128/JB.01578-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Plumlee, C. R., Lee, C., Beg, A. A., Decker, T., Shuman, H. A., Schindler, C. (2009). Interferons Direct an Effective Innate Response to Legionella pneumophila Infection. J. Biol. Chem. 284: 30058-30066 [Abstract] [Full Text]  


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