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Journal of Bacteriology, February 2007, p. 1382-1389, Vol. 189, No. 4
0021-9193/07/$08.00+0     doi:10.1128/JB.01144-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Regulation of Gene Expression in Streptococcus pneumoniae by Response Regulator 09 Is Strain Dependent{triangledown} ,{dagger}

Wouter T. Hendriksen,1 Nuno Silva,2 Hester J. Bootsma,3 Clare E. Blue,2 Gavin K. Paterson,2,{ddagger} Alison R. Kerr,2 Anne de Jong,4 Oscar P. Kuipers,4 Peter W. M. Hermans,1,3* and Tim J. Mitchell2

Department of Pediatrics, Erasmus MC-Sophia Children's Hospital, Rotterdam, The Netherlands,1 Division of Infection and Immunity, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, United Kingdom,2 Laboratory of Pediatric Infectious Diseases, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands,3 Department of Molecular Genetics, University of Groningen, Haren, The Netherlands4

Received 28 July 2006/ Accepted 25 October 2006

Recent murine studies have demonstrated that the role of response regulator 09 (RR09) of Streptococcus pneumoniae in virulence is different in different strains. In the present study, we used a murine pneumonia model of infection to assess the virulence of a TIGR4 rr09 mutant, and we found that TIGR4{Delta}rr09 was attenuated after intranasal infection. Furthermore, we investigated the in vitro transcriptional changes in pneumococcal rr09 mutants of two strains, D39 and TIGR4, by microarray analysis. The transcriptional profiles of the rr09 mutants of both strains had clear differences compared to the profiles of the parental wild-type strains. In D39{Delta}rr09, but not in TIGR4{Delta}rr09, genes involved in competence (e.g., comAB) were upregulated. In TIGR4, genes located on the rlrA pathogenicity islet, which are not present in the D39 genome, appeared to be regulated by RR09. Furthermore, several phosphotransferase systems (PTSs) believed to be involved in sugar uptake (e.g., the PTS encoded by sp0060 to sp0066) were strongly downregulated in D39{Delta}rr09, while they were not regulated by RR09 in TIGR4. To examine the role of one of these PTSs in virulence, D39{Delta}sp0063 was constructed and tested in a murine infection model. No difference between the virulence of this strain and the virulence of the wild type was found, indicating that downregulation of the sp0063 gene alone is not the cause of the avirulent phenotype of D39{Delta}rr09. Finally, expression of rr09 and expression of three of our identified RR09 targets during infection in mice were assessed. This in vivo experiment confirmed that there were differences between expression in wild-type strain TIGR4 and expression in the rr09 mutant, as well as differences between expression in wild-type strain D39 and expression in wild-type strain TIGR4. In conclusion, our results indicate that there is strain-specific regulation of pneumococcal gene expression by RR09.

* Corresponding author. Mailing address: Laboratory of Pediatric Infectious Diseases, Radboud University Nijmegen Medical Centre, P.O. Box 9101 (Route 224), 6500 HB Nijmegen, The Netherlands. Phone: (31)-24-3666406. Fax: (31)-24-3666352. E-mail: P.Hermans{at}cukz.umcn.nl.

{triangledown} Published ahead of print on 3 November 2006.

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

{ddagger} Present address: Biomedical Sciences, DSTL, Porton Down, Salisbury, SP04 0QJ United Kingdom.

Journal of Bacteriology, February 2007, p. 1382-1389, Vol. 189, No. 4
0021-9193/07/$08.00+0     doi:10.1128/JB.01144-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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