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Journal of Bacteriology, August 2007, p. 5976-5986, Vol. 189, No. 16
0021-9193/07/$08.00+0     doi:10.1128/JB.00592-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Staphylococcus aureus ArcR Controls Expression of the Arginine Deiminase Operon ^,

Julia Makhlin,^1, Tzili Kofman,^1, Ilya Borovok,¹ Christian Kohler,² Susanne Engelmann,² Gerald Cohen,¹ and Yair Aharonowitz^1*

Department of Molecular Microbiology and Biotechnology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel,¹ Institut für Mikrobiologie, Ernst Moritz Arndt Universität, F. L. Jahn Str. 15, D-17487 Greifswald, Germany²

Received 17 April 2007/ Accepted 29 May 2007

We identified a single open reading frame that is strongly similar to ArcR, a member of the Crp/Fnr family of bacterial transcriptional regulators, in all sequenced Staphylococcus aureus genomes. The arcR gene encoding ArcR forms an operon with the arginine deiminase (ADI) pathway genes arcABDC that enable the utilization of arginine as a source of energy for growth under anaerobic conditions. In this report, we show that under anaerobic conditions, S. aureus growth is subject to glucose catabolic repression and is enhanced by arginine. Likewise, glucose and arginine have reciprocal effects on the transcription of the arcABDCR genes. Furthermore, we show using a mutant deleted for arcR that the transcription of the arc operon under anaerobic conditions depends strictly on a functional ArcR. These findings are supported by proteome analyses, which showed that under anaerobic conditions the expression of the ADI catabolic proteins depends on ArcR. Bioinformatic analysis of S. aureus ArcR predicts an N-terminal nucleotide binding domain and a C-terminal helix-turn-helix DNA binding motif. ArcR binds to a conserved Crp-like sequence motif, TGTGA-N₆-TCACA, present in the arc promoter region and thereby activates the expression of the ADI pathway genes. Crp-like sequence motifs were also found in the regulatory regions of some 30 other S. aureus genes mostly encoding anaerobic enzymatic systems, virulence factors, and regulatory systems. ArcR was tested and found to bind to the regulatory regions of four such genes, adh1, lctE, srrAB, and lukM. In one case, for lctE, encoding L-lactate dehydrogenase, ArcR was able to bind only in the presence of cyclic AMP. These observations suggest that ArcR is likely to play an important role in the expression of numerous genes required for anaerobic growth.

Published ahead of print on 8 June 2007.

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

J.M. and T.K. contributed equally to this paper.

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