Interplay between three global regulatory proteins mediates oxygen regulation of the Escherichia coli cytochrome d oxidase (cydAB) operon.
The Escherichia coli cydAB operon, encoding the subunits of the high-affinity cytochrome d oxidase, is maximally transcribed in microaerobiosis as a result of the combined action of the oxygen-responsive regulators Fnr and ArcA. Here, we report that the histone-like protein H-NS is an aerobic repressor of cydAB expression. ArcA is shown to antagonize H-NS action to render cydAB expression insensitive to H-NS repression in anaerobiosis. The targets for H-NS-mediated aerobic repression are the four oxygen-regulated promoters, designated P1, P2, P3 and P4. H-NS control is the result of H-NS binding to an extended region within the cydAB promoter element, including sequences upstream from and overlapping the four regulated promoters. We propose a regulatory model in which oxygen control of cydAB transcription is mediated by three alternative protein-DNA complexes that are assembled sequentially on the promoter region as the cells are shifted from aerobic to microaerobic and to anaerobic conditions. According to this model, ArcA-P plays a central role in cydAB regulation by antagonizing H-NS repression of cydAB transcription when oxygen becomes limiting. This allows peak gene expression and subsequent repression by Fnr under fully anaerobic conditions.
Govantes
F
F
Department of Microbiology, Immunology and Molecular Genetics, and the Molecular Biology Institute, 1602 Molecular Sciences Building, University of California, Los Angeles, CA 90095-1489, USA.
Orjalo
A V
AV
Gunsalus
R P
RP
D001426:Bacterial Proteins; D001483:Base Sequence; D017937:Cytochrome d Group / Q000235:genetics*; D017931:DNA Primers; D004268:DNA-Binding Proteins / Q000502:physiology; D004926:Escherichia coli / Q000201:enzymology*; D009876:Operon; D010100:Oxygen / Q000378:metabolism*; D011401:Promoter Regions, Genetic; D014158:Transcription, Genetic / Q000502:physiology
D001426:Bacterial Proteins; D017931:DNA Primers; D004268:DNA-Binding Proteins; C031908:H-NS protein, bacteria; D017937:Cytochrome d Group; D010100:Oxygen