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J. Biol. Chem., Vol. 279, Issue 40, 41546-41556, October 1, 2004

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Synthesis of Mosaic Peptidoglycan Cross-bridges by Hybrid Peptidoglycan Assembly Pathways in Gram-positive Bacteria^*

Ana Arbeloa, Jean-Emmanuel Hugonnet, Anne-Charlotte Sentilhes, Nathalie Josseaume, Lionnel Dubost¶, Christelle Monsempes, Didier Blanot||, Jean-Paul Brouard¶, and Michel Arthur**

From the INSERM E0004, Laboratoire de Recherche Moléculaire sur les Antibiotiques, 15 rue de l'Ecole de Médecine, 75270 Paris, cedex 06, France, ^¶Développement et Diversité Moléculaire, Muséum National d'Histoire Naturelle, USM0502-CNRS UMR8041, 75005 Paris, France, and ^||Enveloppes Bactériennes et Antibiotiques, UMR 8619 CNRS, Btiment 430, Université de Paris-Sud, 91405 Orsay, France

The peptidoglycan cross-bridges of Staphylococcus aureus, Enterococcus faecalis, and Enterococcus faecium consist of the sequences Gly₅, L-Ala₂, and D-Asx, respectively. Expression of the fmhB, femA, and femB genes of S. aureus in E. faecalis led to the production of peptidoglycan precursors substituted by mosaic side chains that were efficiently used by the penicillin-binding proteins for cross-bridge formation. The Fem transferases were specific for incorporation of glycyl residues at defined positions of the side chains in the absence of any additional S. aureus factors such as tRNAs used for amino acid activation. The PBPs of E. faecalis displayed a broad substrate specificity because mosaic side chains containing from 1 to 5 residues and Gly instead of L-Ala at the N-terminal position were used for peptidoglycan cross-linking. Low affinity PBP2a of S. aureus conferred -lactam resistance in E. faecalis and E. faecium, thereby indicating that there was no barrier to heterospecific expression of resistance caused by variations in the structure of peptidoglycan precursors. Thus, conservation of the structure of the peptidoglycan cross-bridges in members of the same species reflects the high specificity of the enzymes for side chain synthesis, although this is not essential for the activity of the PBPs.

Received for publication, June 25, 2004 , and in revised form, July 26, 2004.

^* This work was supported by the programs Action Concertée Incitatrice Microbiologie 2003 from the Fonds National de la Science and Combating Bacterial Resistance to Antibiotics Contract LSHM-CT-2003-503335, 6th PCRD from the European Community. 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.

Recipient of a fellowship from the Gobierno Vasco.

^** To whom correspondence should be addressed: LRMA-E0004, Université Paris VI, 15 rue de l'Ecole de Médecine, 75270 Paris cedex 06, France. Tel.: 33-1-43-25-00-33; Fax: 33-1-43-25-68-12; E-mail: michel.arthur{at}bhdc.jussieu.fr.

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