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NrdR Controls Differential Expression of the Escherichia coli Ribonucleotide Reductase Genes ^,

Eduard Torrents,^1,, Inna Grinberg,^2, Batia Gorovitz-Harris,² Hanna Lundström,¹ Ilya Borovok,² Yair Aharonowitz,² Britt-Marie Sjöberg,^1* and Gerald Cohen^2*

Department of Molecular Biology and Functional Genomics, Stockholm University, SE-10691 Stockholm, Sweden,¹ Department of Molecular Microbiology and Biotechnology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel²

Received 25 March 2007/ Accepted 1 May 2007

Escherichia coli possesses class Ia, class Ib, and class III ribonucleotide reductases (RNR). Under standard laboratory conditions, the aerobic class Ia nrdAB RNR genes are well expressed, whereas the aerobic class Ib nrdEF RNR genes are poorly expressed. The class III RNR is normally expressed under microaerophilic and anaerobic conditions. In this paper, we show that the E. coli YbaD protein differentially regulates the expression of the three sets of genes. YbaD is a homolog of the Streptomyces NrdR protein. It is not essential for growth and has been renamed NrdR. Previously, Streptomyces NrdR was shown to transcriptionally regulate RNR genes by binding to specific 16-bp sequence motifs, NrdR boxes, located in the regulatory regions of its RNR operons. All three E. coli RNR operons contain two such NrdR box motifs positioned in their regulatory regions. The NrdR boxes are located near to or overlap with the promoter elements. DNA binding experiments showed that NrdR binds to each of the upstream regulatory regions. We constructed deletions in nrdR (ybaD) and showed that they caused high-level induction of transcription of the class Ib RNR genes but had a much smaller effect on induction of transcription of the class Ia and class III RNR genes. We propose a model for differential regulation of the RNR genes based on binding of NrdR to the regulatory regions. The model assumes that differences in the positions of the NrdR binding sites, and in the sequences of the motifs themselves, determine the extent to which NrdR represses the transcription of each RNR operon.

Published ahead of print on 11 May 2007.

Supplemental material for this article may be found at http://jb.asm.org/.

Present address: Institute for Bioengineering of Catalonia (IBEC) and Microbiology Department Edifici Anexe—Laboratory 4, Biology Faculty, Avinguda Diagonal 645, 08028 Barcelona, Spain.

E.T. and I.G. contributed equally to this study.