Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors.

The electron-transport chains of Escherichia coli are composed of many different dehydrogenases and terminal reductases (or oxidases) which are linked by quinones (ubiquinone, menaquinone and demethylmenaquinone). Quinol:cytochrome c oxido-reductase ('bc1 complex') is not present. For various electron acceptors (O2, nitrate) and donors (formate, H2, NADH, glycerol-3-P) isoenzymes are present. The enzymes show great variability in membrane topology and energy conservation. Energy is conserved by conformational proton pumps, or by arrangement of substrate sites on opposite sides of the membrane resulting in charge separation. Depending on the enzymes and isoenzymes used, the H+/e- ratios are between 0 and 4 H+/e- for the overall chain. The expression of the terminal reductases is regulated by electron acceptors. O2 is the preferred electron acceptor and represses the terminal reductases of anaerobic respiration. In anaerobic respiration, nitrate represses other terminal reductases, such as fumarate or DMSO reductases. Energy conservation is maximal with O2 and lowest with fumarate. By this regulation pathways with high ATP or growth yields are favoured. The expression of the dehydrogenases is regulated by the electron acceptors, too. In aerobic growth, non-coupling dehydrogenases are expressed and used preferentially, whereas in fumarate or DMSO respiration coupling dehydrogenases are essential. Coupling and non-coupling isoenzymes are expressed correspondingly. Thus the rationale for expression of the dehydrogenases is not maximal energy yield, but could be maximal flux or growth rates. Nitrate regulation is effected by two-component signal transfer systems with membraneous nitrate/nitrite sensors (NarX, NarQ) and cytoplasmic response regulators (NarL, NarP) which communicate by protein phosphorylation. O2 regulates by a two-component regulatory system consisting of a membraneous sensor (ArcB) and a response regulator (ArcA). ArcA is the major regulator of aerobic metabolism and represses the genes of aerobic metabolism under anaerobic conditions. FNR is a cytoplasmic O2 responsive regulator with a sensory and a regulatory DNA-binding domain. FNR is the regulator of genes required for anaerobic respiration and related pathways. The binding sites of NarL, NarP, ArcA and FNR are characterized for various promoters. Most of the genes are regulated by more than one of the regulators, which can act in any combination and in a positive or negative mode. By this the hierarchical expression of the genes in response to the electron acceptors is achieved. FNR is located in the cytoplasm and contains a 4Fe4S cluster in the sensory domain. The regulatory concentrations of O2 are 1-5 mbar. Under these conditions O2 diffuses to the cytoplasm and is able to react directly with FNR without involvement of other specific enzymes or protein mediators. By oxidation of the FeS cluster, FNR is converted to the inactive state in a reversible process. Reductive activation could be achieved by cellular reductants in the absence of O2. In addition, O2 may cause destruction and loss of the FeS cluster. It is not known whether this process is required for regulation of FNR function.

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