Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli: Study utilizing deletions and lac fusions of cyo and cyd

Escherichia coli has two terminal oxidases for its respiratory chain: cytochrome o (low O₂ affinity) and cytochrome d (high O₂ affinity). Expression of the cyo operon, encoding cytochrome o, is decreased by anaerobic growth, whereas expression of the cyd operon, encoding cytochrome d, is increased by anaerobic growth. We show by the use of lac gene fusion that the expressions of cyo and cyd are under the control of the two-component arc system. In a cyo⁺ cyd⁺ background, expression of Φ(cyo-lac) is higher when the organism is grown aerobically than when it is grown anaerobically. A mutation in either the sensor gene arcB or the pleiotropic regulator gene arcA almost abolishes the anaerobic repression. In the same background, expression of Φ(cyd-lac) is higher under anaerobic growth conditions than under aerobic growth conditions. A mutation in arcA or arcB lowers both the aerobic and anaerobic expressions, suggesting that ArcA plays an activating role instead of the typical repressing role. Under aerobic growth conditions, double deletions of cyo and cyd lower Φ(cyo-lac) expression but enhance Φ(cyd-lac) expression. The double deletions also prevent elevated aerobic induction of the lct operon (encoding L-lactate dehydrogenase), another target operon of the arc system. In contrast, these deletions do not circumvent aerobic repression of the nar operon (encoding the anaerobic respiratory enzyme nitrate reductase) under the control of the pleiotropic fnr gene product. It thus appears that ArcB senses the presence of O₂ by the level of an electron transport component in reduced form or that of a nonautoxidizable compound linked to the process by a redox reaction, whereas Fnr senses O₂ by a different mechanism.