The aerobic respiratory chain of Escherichia coli contains two terminal
oxidases that catalyze the oxidation of ubiquinol-8 and the reduction of
oxygen to water. They are the
cytochrome o oxidase complex encoded by cyoABCDE and the
cytochrome d oxidase complex encoded by cydAB. To determine how these genes are regulated in response to a variety of environmental stimuli, including
oxygen, we examined their expression by using lacZ
protein fusions in wild-type and fnr mutant strains of E. coli. Anaerobic growth resulted in a 140-fold repression of cyoA'-'lacZ expression relative to aerobic growth and a 3-fold increase in cydA'-'lacZ expression. Anaerobic repression of both fusions was mediated in part by the fnr gene product, as evidenced by a 30-fold derepression of cyoA'-'lacZ expression and a 4-fold derepression of cydA'-'lacZ expression in an fnr deletion strain. Supplying wild-type fnr in trans restored wild-type repression for both fusions. Fnr thus functions as an anaerobic repressor of both cyoABCDE and cydAB expression. Reduced-minus-oxidized difference spectrum analyses of cell membranes confirmed the effect of the fnr gene product on the production of
cytochrome d oxidase in the cell. Based on the pattern of anaerobic cydAB expression observed, we propose the existence of a second, as yet unidentified, regulatory
element that must function either to activate cydAB expression as
oxygen becomes limiting or to repress cydAB expression aerobically. Whereas
cytochrome o oxidase encoded by cyoABCDE appears to be produced only under
oxygen-rich growth conditions, in keeping with its biochemical properties,
cytochrome d oxidase is expressed moderately aerobically and is elevated yet further when
oxygen becomes limiting so that the organism can cope better under
oxygen starvation conditions. We also examined cyoABCDE and cydAB expression in response to growth on alternative
carbon compounds and to changes in the culture medium pH and osmolarity.