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Originally published In Press as doi:10.1074/jbc.M101109200 on September 13, 2001

J. Biol. Chem., Vol. 276, Issue 47, 44297-44306, November 23, 2001
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Pleiotropic Functions of a Streptomyces pristinaespiralis Autoregulator Receptor in Development, Antibiotic Biosynthesis, and Expression of a Superoxide Dismutase*

Marc Folcher, Hélène GaillardDagger , Lieu T. Nguyen, Kien T. Nguyen, Patricia Lacroix§, Nathalie Bamas-Jacques§, Monique Rinkel, and Charles J. Thompson||

From the Department of Molecular Microbiology, Biocenter, 70 Klingelbergstrasse, University of Basel, 4056 Basel, Switzerland

In Streptomyces, a family of related butyrolactones and their corresponding receptor proteins serve as quorum-sensing systems that can activate morphological development and antibiotic biosynthesis. Streptomyces pristinaespiralis contains a gene cluster encoding enzymes and regulatory proteins for the biosynthesis of pristinamycin, a clinically important streptogramin antibiotic complex. One of these proteins, PapR1, belongs to a well known family of Streptomyces antibiotic regulatory proteins. Gel shift assays using crude cytoplasmic extracts detected SpbR, a developmentally regulated protein that bound to the papR1 promoter. SpbR was purified, and its gene was cloned using reverse genetics. spbR encoded a 25-kDa protein similar to Streptomyces autoregulatory proteins of the butyrolactone receptor family, including scbR from Streptomyces coelicolor. In Escherichia coli, purified SpbR and ScbR produced bound sequences immediately upstream of papR1, spbR, and scbR. SpbR DNA-binding activity was inhibited by an extracellular metabolite with chromatographic properties similar to those of the well known gamma -butyrolactone signaling compounds. DNase I protection assays mapped the SpbR-binding site in the papR1 promoter to a sequence homologous to other known butyrolactone autoregulatory elements. A nucleotide data base search showed that these binding motifs were primarily located upstream of genes encoding Streptomyces antibiotic regulatory proteins and butyrolactone receptors in various Streptomyces species. Disruption of the spbR gene in S. pristinaespiralis resulted in severe defects in growth, morphological differentiation, pristinamycin biosynthesis, and expression of a secreted superoxide dismutase.

* This work was supported by Aventis Pharma S. A. and the University of Basel.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EMBL Data Bank with accession number(s) AY026762.

Dagger Present address: Inst. of Cell Biology, Eidgenössisch Technische Hochschule Hönggerberg, 8093 Zürich, Switzerland.

§ Present address: Aventis Pharma S. A., 13 quai Jules Guesde, 94403 Vitry-sur-Seine, Cedex France.

Present address: Bio Media, Zone Industrielle du Bousquet, 31360 Boussens, France.

|| To whom correspondence should be addressed. Tel.: 41-61-267-2116; Fax: 41-61-267-2118; E-mail: charles-j.thompson@unibas.ch.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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