Inter-chain transacylation of d-alanine ester residues of lipoteichoic acid: a unique mechanism of membrane communication

Abstract

Lipoteichoic acid is an important example of an amphiphile that appears to play a vital role in bacterial growth. A number of functions have been ascribed to this polymer. These include the regulation of autolytic enzymes, the binding of Mgz+ for enzyme function, and the assembly of wall polymers. One of the key components which has been proposed to modulate these functions is the substituent D-alanine. James Baddiley and his co-workers discovered that this amino acid is an important component of most teichoic acids (Armstrong et al., 1959). Thus, esterification of teichoic acids by D-alanine may be an important step in controlling the function of this polymer in wall assembly. In Lactobacillus casei the incorporation of D-alanine into lipoteichoic acid is accomplished in a two-step reaction sequence. The first step of this sequence was discovered in 1960 when Baddiley & Neuhaus showed that a variety of Gram-positive organisms have the ability to activate Dalanine. The second step of this sequence was not detected until Reusch & Neuhaus (1971) recognized that the incorporation of D-alanine into teichoic acids in vitro required the endogenous membrane teichoic acid to act as acceptor. All attempts to demonstrate the incorporation of D-alanine into isolated wall teichoic acid proved to be elusive and it was reasoned that the teichoic acid has to be intimately associated with the membrane in a particular conformation or environment (Neuhaus et aZ., 1974). On the basis of this hypothesis a system for the incorporation of D-alanine into membranes was found that required both a supernatant fraction and ATP, and was stimulated by metal ions. Linzer & Neuhaus (1973) showed that the supernatant fraction could be replaced by the D-alanine-activating enzyme and a protein factor designated D-alanine: membrane acceptor ligase. L. casei was chosen for these experiments because, firstly, it has a high concentration of the Abbreviation used: LTA, lipoteichoic acid. *Dedicated to Sir James Baddiley.

A Continuum of Anionic Charge: Structures and Functions ofd-Alanyl-Teichoic Acids in Gram-Positive Bacteria

“…15, it is proposed that this process of inter-and intrachain transacylation is responsible for modulating the net anionic charge and lipophilicity of the hydrophilic LTA chain. In this way, perturbation of the D-alanyl ester content by either acylation or deacylation at one location in the membrane can be translated to an adjacent location (365). The proposal does not account for differences in the degree of D-alanylation of short-chain and longchain LTA noted above.…”

Domains in the S‐layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self‐assembly

“…The His‐CbsA peptide 251–410 bound to cells of L. casei , whereas peptide 288–410 was inactive with L. casei cells. This may indicate that region 251–287 modulates the binding of the C‐terminus to teichoic acids and LTA, and the observed differential binding may be related to the reported lack of teichoic acids in the cell wall of L. casei (Neuhaus et al ., 1985). We also found that the two C‐terminal peptides did not bind to all lactobacillar cell walls.…”

d -Alanylation of Lipoteichoic Acid: Role of the d -Alanyl Carrier Protein in Acylation

“…The ability of Dcp to effect the transacylation of these ester residues in the cell wall matrix could provide a mechanism for modulating surface charge and hence ligand binding and autolysin activity. While transacylation of D-alanyl esters was reported between short-chain LTA and long-chain LTA (2,19), the rate of this reaction was relatively slow. Thus, it is hypothesized that transacylation in the presence of Dcp is accelerated and hence Dcp plays a major role in distributing D-alanine esters from one location of the wall matrix to another.…”