The cytochrome bd oxidase of Escherichia coli prevents respiratory inhibition by endogenous and exogenous hydrogen sulfide

• Published in: Molecular microbiology 2016-07, Vol.101 (1), p.62-77
• Main Authors: Korshunov, Sergey, Imlay, Karin R. C., Imlay, James A.
• Format: Article
• Language: English
• Subjects: Cytochrome; Cytochromes - metabolism; E coli; Electron Transport Chain Complex Proteins - metabolism; Electron Transport Complex IV - metabolism; Escherichia coli; Escherichia coli - drug effects; Escherichia coli - enzymology; Escherichia coli - metabolism; Escherichia coli Proteins - metabolism; Hydrogen sulfide; Hydrogen Sulfide - metabolism; Hydrogen Sulfide - pharmacology; Oxidoreductases - metabolism; Oxygen - metabolism; Oxygen Consumption - physiology; Respiration; Sulfur
• ISSN: 0950-382X; 1365-2958
• DOI: 10.1111/mmi.13372

Summary When sulfur compounds are scarce or difficult to process, Escherichia coli adapts by inducing the high‐level expression of sulfur‐compound importers. If cystine then becomes available, the cystine is rapidly overimported and reduced, leading to a burgeoning pool of intracellular cysteine. Most of the excess cysteine is exported, but some is adventitiously degraded, with the consequent release of sulfide. Sulfide is a potent ligand of copper and heme moieties, raising the prospect that it interferes with enzymes. We observed that when cystine was provided and sulfide levels rose, E. coli became strictly dependent upon cytochrome bd oxidase for continued respiration. Inspection revealed that low‐micromolar levels of sulfide inhibited the proton‐pumping cytochrome bo oxidase that is regarded as the primary respiratory oxidase. In the absence of the back‐up cytochrome bd oxidase, growth failed. Exogenous sulfide elicited the same effect. The potency of sulfide was enhanced when oxygen concentrations were low. Natural oxic‐anoxic interfaces are often sulfidic, including the intestinal environment where E. coli dwells. We propose that the sulfide resistance of the cytochrome bd oxidase is a key trait that permits respiration in such habitats. Toxic levels of intracellular sulfide arise either from the degradation of excess cysteine or from an influx of hydrogen sulfide itself. Sulfide inhibits the primary respiratory cytochrome bo oxidase, and continued respiration depends upon the presence of the secondary cytochrome bd oxidase. This scenario is likely common to sulfidic environments, such as the mammalian gut.