Regulation of D-Alanyl-Lipoteichoic Acid Biosynthesis in Streptococcus agalactiae Involves a Novel Two-Component Regulatory System

doi:10.1128/JB.183.21.6324-6334.2001

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Journal of Bacteriology, November 2001, p. 6324-6334, Vol. 183, No. 21
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.21.6324-6334.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Regulation of D-Alanyl-Lipoteichoic Acid Biosynthesis in Streptococcus agalactiae Involves a Novel Two-Component Regulatory System

Claire Poyart,¹^,² Marie Cécile Lamy,¹ Claire Boumaila,¹ Franz Fiedler,³ and Patrick Trieu-Cuot¹^,²^,^*

Laboratoire de Microbiologie, INSERM U-411¹ and Laboratoire Mixte Pasteur-Necker de Recherche sur les Streptocoques et Streptococcies,² Faculté de Médecine Necker-Enfants Malades, 75730 Paris Cedex 15, France, and Institute for Genetics and Microbiology, University of Munich, D-80638 Munich, Germany³

Received 16 April 2001/Accepted 8 August 2001

The dlt operon of gram-positive bacteria comprises four genes (dltA, dltB, dltC, and dltD) that catalyze the incorporationof D-alanine residues into the lipoteichoic acids (LTAs). In thiswork, we characterized the dlt operon of Streptococcus agalactiae,which, in addition to the dltA to dltD genes, included two regulatorygenes, designated dltR and dltS, located upstream of dltA. ThedltR gene encodes a 224-amino-acid putative response regulatorbelonging to the OmpR family of regulatory proteins. The dltSgene codes for a 395-amino-acid putative histidine kinase thoughtto be involved in the sensing of environmental signals. The dltoperon of S. agalactiae is mainly transcribed from the P_dltRpromoter, which directs synthesis of a 6.5-kb transcript encompassingdltR, dltS, dltA, dltB, dltC, and dltD, and from a weaker promoter,P_dltA, which is located in the 3' extremity of dltS.We demonstrate that P_dltR, but not P_dlA, isactivated by DltR in the presence of DltS in D-Ala-deficient LTAmutants resulting from insertional inactivation of the dltA gene,which encodes the cytoplasmic D-alanine-D-alanyl carrier ligaseDltA. Expression of the dlt operon does not require DltR and DltS,since the basal activity of P_dltR is high, being 20-foldthat of the constitutive promoter P_aphA-3 which directssynthesis of the kanamycin resistance gene aphA-3 in various gram-positivebacteria. We hypothesize that the role of DltR and DltS in thecontrol of expression of the dlt operon is to maintain the levelof D-Ala esters in LTAs at a constant and appropriate value whateverthe environmental conditions. The DltA mutant displayed the ability to form clumps in standing cultureand exhibited an increased susceptibility to the cationic antimicrobialpolypeptidecolistin.

^* Corresponding author. Mailing address: Laboratoire de Microbiologie, Faculté de Médecine Necker-Enfants Malades, 75730 ParisCedex 15, France. Phone: (33)(1)40 61 56 79. Fax: (33)(1)40 6155 92. E-mail: ptrieu{at}pasteur.fr.

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