Abstract
Oxygen availability is the major determinant of the metabolic modes adopted by Escherichia coli. Although much is known about E. coli gene expression and metabolism under fully aerobic and anaerobic conditions, the intermediate oxygen tensions that are encountered in natural niches are understudied. Here, for the first time, the transcript profiles of E. coli K-12 across the physiologically significant range of oxygen availabilities are described. These suggested a progressive switch to aerobic respiratory metabolism and a remodeling of the cell envelope as oxygen availability increased. The transcriptional responses were consistent with changes in the abundance of cytochrome bd and bo' and the outer membrane protein OmpW. The observed transcript and protein profiles result from changes in the activities of regulators that respond to oxygen itself or to metabolic and environmental signals that are sensitive to oxygen availability (aerobiosis). A probabilistic model (TFInfer) was used to predict the activity of the indirect oxygen-sensing two-component system ArcBA across the aerobiosis range. The model implied that the activity of the regulator ArcA correlated with aerobiosis but not with the redox state of the ubiquinone pool, challenging the idea that ArcA activity is inhibited by oxidized ubiquinone. The amount of phosphorylated ArcA correlated with the predicted ArcA activities and with aerobiosis, suggesting that fermentation product-mediated inhibition of ArcB phosphatase activity is the dominant mechanism for regulating ArcA activity under the conditions used here.
Highlights
Many environments, both natural and man-made, are characterized by the presence of oxygen gradients and/or regions of variable oxygen availability
As indicated by Alexeeva et al [5], in the relatively few attempts to study E. coli grown at intermediate oxygen tensions, it was apparent that neither dissolved oxygen tension nor the gas input to a chemostat accurately describes the responses of the culture to changes in oxygen availability
Analyzing cultures at fixed points on the aerobiosis scale allows the responses of E. coli K-12 to environments with different oxygen availabilities to be accurately measured and compared, but this has never been exploited for transcriptomic profiling
Summary
For the first time, carefully controlled chemostat cultures have been used to systematically study the effects of oxygen availability on the transcriptome, redox state of the ubiquinone/ubiquinol pool, outer membrane protein profiles, and terminal oxidase proteins of E. coli K-12. The activity of ArcA inferred from the transcript profiles using TFInfer [22] did not correlate with the redox state of the ubiquinone/ubiquinol pool. This prompted experiments to measure the amounts of phosphorylated ArcA, which did correlate well with ArcA activity predicted by the model. This implies that the redox state of the ubiquinone pool is not a major factor in switching ArcA between active and inactive states under the conditions used here, but rather that ArcA activity decreases as aerobiosis increases
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