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Journal of Bacteriology, November 2000, p. 6055-6065, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Defects in D-Alanyl-Lipoteichoic Acid Synthesis in Streptococcus mutans Results in Acid Sensitivity

David A. Boyd,1 Dennis G. Cvitkovitch,2,3 Arnold S. Bleiweis,3 Michael Y. Kiriukhin,4 Dmitri V. Debabov,4 Francis C. Neuhaus,4 and Ian R. Hamilton1,*

Department of Oral Biology, University of Manitoba, Winnipeg, Manitoba R3E 0W2,1 and Dental Research Institute, Faculty of Dentistry, University of Toronto, Toronto, Ontario M5G 1G6,2 Canada; Department of Oral Biology, University of Florida, Gainesville, Florida 326103; and Department of Biochemistry, Molecular and Cell Biology, Northwestern University, Evanston, Illinois 602084

Received 20 March 2000/Accepted 3 August 2000

In the cariogenic organism, Streptococcus mutans, low pH induces an acid tolerance response (ATR). To identify acid-regulated proteins comprising the ATR, transposon mutagenesis with the thermosensitive plasmid pGh9:ISS1 was used to produce clones that were able to grow at neutral pH, but not in medium at pH 5.0. Sequence analysis of one mutant (IS1A) indicated that transposition had created a 6.3-kb deletion, one end of which was in dltB of the dlt operon encoding four proteins (DltA-DltD) involved in the synthesis of D-alanyl-lipoteichoic acid. Inactivation of the dltC gene, encoding the D-alanyl carrier protein (Dcp), resulted in the generation of the acid-sensitive mutant, BH97LC. Compared to the wild-type strain, LT11, the mutant exhibited a threefold-longer doubling time and a 33% lower growth yield. In addition, it was unable to initiate growth below pH 6.5 and unadapted cells were unable to survive a 3-h exposure in medium buffered at pH 3.5, while a pH of 3.0 was required to kill the wild type in the same time period. Also, induction of the ATR in BH97LC, as measured by the number of survivors at a pH killing unadapted cells, was 3 to 4 orders of magnitude lower than that exhibited by the wild type. While the LTA of both strains contained a similar average number of glycerolphosphate residues, permeabilized cells of BH97LC did not incorporate D-[14C]alanine into this amphiphile. This defect was correlated with the deficiency of Dcp. Chemical analysis of the LTA purified from the mutant confirmed the absence of D-alanine-esters. Electron micrographs showed that BH97LC is characterized by unequal polar caps and is devoid of a fibrous extracellular matrix present on the surface of the wild-type cells. Proton permeability assays revealed that the mutant was more permeable to protons than the wild type. This observation suggests a mechanism for the loss of the characteristic acid tolerance response in S. mutans.

* Corresponding author. Mailing address: Department of Oral Biology, University of Manitoba, Winnipeg, Manitoba R3E 0W2, Canada. Phone: (204) 789-3615. Fax: (204) 789-3948. E-mail: ihamilt{at}umanitoba.ca.

Journal of Bacteriology, November 2000, p. 6055-6065, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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