Organization of the respiratory chain of Neisseria meningitidis

Abstract

The ability of Neisseria meningitidis to utilize both oxygen and nitrogen oxides as respiratory substrates allows it to thrive in the diverse environment of the human host. Genome analysis highlighted genes encoding a cbb(3) cytochrome oxidase, the aniA nitrite reductase gene and the norB nitric oxide reductase gene. In the present study, we used myxothiazol as an inhibitor of the bc(1) complex in intact cells and demonstrated that electron flow to nitrite reductase and the cytochrome oxidase, but not NO reductase, passes via the cytochrome bc(1) complex. UV-visible spectrophotometry of intact cells demonstrated that oxygen oxidizes c-type and b-type cytochromes. Oxidation of cytochromes by nitrite was only seen in microaerobically precultured whole cells, and the predominant oxidizable cytochromes were b-type. These are likely to be associated with the oxidation of a b-haem-containing nitric oxide reductase. Nitrite inhibits the oxidation of cytochromes by oxygen in a nitrite reductase-independent manner, indicating that nitrite may inhibit oxidase activity directly, as well as via the intermediate of denitrification, nitric oxide.

Organization of the Electron Transfer Chain to Oxygen in the Obligate Human Pathogen Neisseria gonorrhoeae : Roles for Cytochromes c 4 and c 5 , but Not Cytochrome c 2 , in Oxygen Reduction

“…A seventh c-type cytochrome, Ccp, is expressed at low levels during oxygen-limited growth (21,47,53). However, cytochrome c 2 has not been visualized either in gonococci or in the closely related pathogen Neisseria meningitidis (4); consequently, its role in gonococcal electron transfer pathways remains to be defined.…”

“…Cytochromes c 4 and c 5 were first identified in the nitrogenfixing bacterium Azotobacter vinelandii, where they were proposed to provide parallel pathways for electron transfer between the cytochrome bc 1 complex and cytochrome oxidase (11). Many years later, it was tentatively suggested that they provide two independent pathways to a cytochrome cbb 3 type of cytochrome oxidase (34).…”

“…In both B. japonicum and the Neisseriaceae, it is encoded by the ccoNOPQ operon (originally designated the fixNOPQ operon, for nitrogen fixation), in which the ccoO and ccoP genes encode c-type cytochromes. Genes for six other gonococcal c-type cytochromes include cycP, encoding cytochrome cЈ, which was implicated in protection against NO toxicity (48); ccp, encoding a cytochrome c peroxidase (47); petC, encoding the cytochrome c 1 component of the cytochrome bc 1 complex; and three genes, cccA, cycA, and cycB, encoding cytochromes of unknown function that have been designated cytochromes c 2 , c 4 , and c 5 , respectively. By staining proteins separated by SDS-PAGE for covalently bound heme, we and others have demonstrated the accumulation of six c-type cytochromes during aerobic growth, including both cytochromes c 4 and c 5 (43,47,48).…”

“…This offers a possible explanation for the conflicting previous proposals concerning the organization of the gonococcal respiratory chain, namely, that there are branched electron transfer pathways to oxygen that diverge at the cytochrome bc 1 complex but terminate with the same cytochrome oxidase, cbb 3 . The current study was therefore designed to determine whether gonococcal cytochromes c 4 and c 5 provide alternative pathways for electron transfer between cytochrome bc 1 and cytochrome oxidase cbb 3 and whether cytochrome c 2 also provides an alternative electron transfer pathway to cytochrome oxidase. The results obtained provide fascinating insights into why a pathogen with a microaerobic life-style maintains such a high respiratory capacity and is a prolific source of electron transfer components.…”

Biochemical and Biophysical Characterization of the Two Isoforms of cbb3-Type Cytochrome c Oxidase from Pseudomonas stutzeri

“…Therefore, for instance, in the symbiotic diazotrophs, cbb 3 -CcOs are needed to provide energy required for the ATP-consuming process of N 2 fixation and may serve to protect the oxygen-sensitive nitrogenase by oxygen scavenging (12). In some human pathogens, e.g., Helicobacter pylori (13) and Neisseria meningitidis (14), the cbb 3 -CcO is the only respiratory oxidase encoded by the genome and is believed to be crucial for the colonization of the hosts under hypoxic conditions (8). In addition to the reduction of molecular oxygen, cbb 3 -CcOs, which are structurally and phylogenetically related to bacterial nitric oxide reductases (NORs) (6,15), were shown to reduce NO (16,17) with a higher turnover number than oxidases from the A and B families (18).…”