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J. Biol. Chem., Vol. 278, Issue 26, 23874-23881, June 27, 2003

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Cell Wall Attachment of a Widely Distributed Peptidoglycan Binding Domain Is Hindered by Cell Wall Constituents^*

Anton Steen , Girbe Buist  , Kees J. Leenhouts ¶, Mohamed El Khattabi ¶, Froukje Grijpstra ¶, Aldert L. Zomer, Gerard Venema, Oscar P. Kuipers and Jan Kok ||

From the Department of Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Kerklaan 30, 9751 NN Haren, The Netherlands and ^¶BioMaDe Technology Foundation, Nijenborgh 4, 9747 AG Groningen, The Netherlands

The C-terminal region (cA) of the major autolysin AcmA of Lactococcus lactis contains three highly similar repeated regions of 45 amino acid residues (LysM domains), which are separated by nonhomologous sequences. The cA domain could be deleted without destroying the cell wall-hydrolyzing activity of the enzyme in vitro. This AcmA derivative was capable neither of binding to lactococcal cells nor of lysing these cells while separation of the producer cells was incomplete. The cA domain and a chimeric protein consisting of cA fused to the C terminus of MSA2, a malaria parasite surface antigen, bound to lactococcal cells specifically via cA. The fusion protein also bound to many other Gram-positive bacteria. By chemical treatment of purified cell walls of L. lactis and Bacillus subtilis, peptidoglycan was identified as the cell wall component interacting with cA. Immunofluorescence studies showed that binding is on specific locations on the surface of L. lactis, Enterococcus faecalis, Streptococcus thermophilus, B. subtilis, Lactobacillus sake, and Lactobacillus casei cells. Based on these studies, we propose that LysM-type repeats bind to peptidoglycan and that binding is hindered by other cell wall constituents, resulting in localized binding of AcmA. Lipoteichoic acid is a candidate hindering component. For L. lactis SK110, it is shown that lipoteichoic acids are not uniformly distributed over the cell surface and are mainly present at sites where no MSA2cA binding is observed.

Received for publication, October 29, 2002 , and in revised form, April 8, 2003.

^* This work was supported in part by Unilever Research Laboratorium (Vlaardingen, The Netherlands). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

These two authors contributed equally to this work.

^|| Recipient of a fellowship of the Royal Netherlands Academy of Arts and Sciences.

To whom corresponding should be addressed. Tel.: 31-50-3632287; Fax: 31-50-3632348; E-mail: g.buist{at}biol.rug.nl.

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