Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments.

Abstract

Upon exposure to oxygen, Escherichia coli increases the expression of enzymes essential for aerobic respiration, such as components of the TCA cycle and terminal oxidase complexes. This increase requires the elimination of repression mediated by the Arc regulatory system under anaerobic conditions. Coordinately, the synthesis of enzymes that function in anaerobic processes such as fermentation decreases, partly due to the inactivation of the transcription factor Fnr. E. coli is thus able to adjust the levels of respiratory enzymes to fit its environmental circumstances, and in this case, reduces the production of the less energy efficient fermentation enzymes in favor of the aerobic pathways. In contrast to the advantage in energy production, aerobiosis brings a disadvantage to E. coli: the production of reactive oxygen species (ROS), i.e. superoxide anion radical (O2.-), hydrogen peroxide (H2O2), and hydroxyl radical (.OH). These byproducts of aerobic respiration damage many biological molecules, including DNA, proteins, and lipids. To alleviate the toxicity of these compounds, E. coli induces the synthesis of protective enzymes, such as Mn-dependent superoxide dismutase (SodA) and catalase I (HP I), and this induction is controlled by the regulatory proteins SoxRS, OxyR, and ArcAB. Thus, ArcAB, Fnr, SoxRS, and OxyR function in concert so that E. coli can optimize its energy production and growth rate. Fnr and SoxRS are cytoplasmic, DNA-binding proteins, and these regulatory systems utilize iron-sulfur clusters as cofactors which may directly sense the redox environment. OxyR is also a cytoplasmic, DNA-binding protein, and appears to respond to redox potential through the oxidation state of a specific cysteine residue. In the ArcAB system (which belongs to the family of two-component regulatory systems), ArcB, a membrane protein, functions as the sensor, and ArcA, a DNA-binding protein, directly controls target gene expression. Under anaerobic conditions, ArcB undergoes autophosphorylation and transphosphorylates ArcA, stimulating ArcA's DNA-binding activity. During aerobic growth, the transphosphorylation of ArcA does not occur. In this signal transduction mechanism, the ArcB C-terminal or "receiver" domain plays a critical role; that is, it stimulates or abolishes the transphosphorylation depending on the metabolic state of the cell, which in turn is influenced by the availability of oxygen. E. coli thus employs at least four global regulatory systems which monitor the cellular oxidative/metabolic conditions, and adjust the expression of more than 70 operons to give the organism a better aerobic life.