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The pathogen Neisseria meningitidis requires oxygen, but supplements growth by denitrification. Nitrite, nitric oxide and oxygen control respiratory flux at genetic and metabolic levels

The pathogen Neisseria meningitidis requires oxygen, but supplements growth by denitrification. Nitrite, nitric oxide and oxygen control respiratory flux at genetic and metabolic levels
The pathogen Neisseria meningitidis requires oxygen, but supplements growth by denitrification. Nitrite, nitric oxide and oxygen control respiratory flux at genetic and metabolic levels

The human pathogen Neisseria meningitidis is the major causative agent of bacterial meningitis. The organism is usually treated as a strict aerobe and is cultured under fully aerobic conditions in the laboratory. We demonstrate here that although N. meningitidis fails to grow under strictly anaerobic conditions, under oxygen limitation the bacterium expresses a denitrification pathway (reduction of nitrite to nitrous oxide via nitric oxide) and that this pathway supplements growth. The expression of the gene aniA, which encodes nitrite reductase, is regulated by oxygen depletion and nitrite availability via transcriptional regulator FNR and two-component sensor-regulator NarQ/NarP respectively. Completion of the two-step denitrification pathway requires nitric oxide (NO) reduction, which proceeds after NO has accumulated during batch growth under oxygen-limited conditions. During periods of NO accumulation both nitrite and NO reduction are observed aerobically, indicating N. meningitidis can act as an aerobic denitrifier. However, under steady-state conditions in which NO is maintained at a low concentration, oxygen respiration is favoured over denitrification. NO inhibits oxidase activity in N. meningitidis with an apparent Ki NO = 380 nM measured in intact cells. The high respiratory flux to nitrite after microaerobic growth and the finding that accumulation of the denitrification intermediate NO inhibits oxygen respiration support the view that denitrification is a pathway of major importance in N. meningitidis.

Adult, Aerobiosis, Bacterial Proteins, Cell Respiration, Gene Expression Regulation, Bacterial, Humans, Infant, Meningococcal Infections, Neisseria meningitidis, Nitric Oxide, Nitrite Reductases, Nitrites, Nitrous Oxide, Oxidation-Reduction, Oxidoreductases, Oxygen, Journal Article, Research Support, Non-U.S. Gov't
0950-382X
800-809
Rock, Jonathan D.
8e8fc55a-ebd8-4fcf-93e7-99b2909d34f0
Mahnane, M. Reda
98f3c0d0-3846-4ab5-82ee-1bae46937571
Anjum, Muna F.
67131223-aacc-4994-a435-baf5ebfb0d95
Shaw, Jonathan G.
4cc7c1a5-4dd2-41cd-a9a2-813a434c8f30
Read, Robert C.
b5caca7b-0063-438a-b703-7ecbb6fc2b51
Moir, James W.B.
f6831b5f-5cfd-4c56-b3cd-6782f413a07f
Rock, Jonathan D.
8e8fc55a-ebd8-4fcf-93e7-99b2909d34f0
Mahnane, M. Reda
98f3c0d0-3846-4ab5-82ee-1bae46937571
Anjum, Muna F.
67131223-aacc-4994-a435-baf5ebfb0d95
Shaw, Jonathan G.
4cc7c1a5-4dd2-41cd-a9a2-813a434c8f30
Read, Robert C.
b5caca7b-0063-438a-b703-7ecbb6fc2b51
Moir, James W.B.
f6831b5f-5cfd-4c56-b3cd-6782f413a07f

Rock, Jonathan D., Mahnane, M. Reda, Anjum, Muna F., Shaw, Jonathan G., Read, Robert C. and Moir, James W.B. (2005) The pathogen Neisseria meningitidis requires oxygen, but supplements growth by denitrification. Nitrite, nitric oxide and oxygen control respiratory flux at genetic and metabolic levels. Molecular Microbiology, 58 (3), 800-809. (doi:10.1111/j.1365-2958.2005.04866.x).

Record type: Article

Abstract

The human pathogen Neisseria meningitidis is the major causative agent of bacterial meningitis. The organism is usually treated as a strict aerobe and is cultured under fully aerobic conditions in the laboratory. We demonstrate here that although N. meningitidis fails to grow under strictly anaerobic conditions, under oxygen limitation the bacterium expresses a denitrification pathway (reduction of nitrite to nitrous oxide via nitric oxide) and that this pathway supplements growth. The expression of the gene aniA, which encodes nitrite reductase, is regulated by oxygen depletion and nitrite availability via transcriptional regulator FNR and two-component sensor-regulator NarQ/NarP respectively. Completion of the two-step denitrification pathway requires nitric oxide (NO) reduction, which proceeds after NO has accumulated during batch growth under oxygen-limited conditions. During periods of NO accumulation both nitrite and NO reduction are observed aerobically, indicating N. meningitidis can act as an aerobic denitrifier. However, under steady-state conditions in which NO is maintained at a low concentration, oxygen respiration is favoured over denitrification. NO inhibits oxidase activity in N. meningitidis with an apparent Ki NO = 380 nM measured in intact cells. The high respiratory flux to nitrite after microaerobic growth and the finding that accumulation of the denitrification intermediate NO inhibits oxygen respiration support the view that denitrification is a pathway of major importance in N. meningitidis.

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More information

Published date: November 2005
Keywords: Adult, Aerobiosis, Bacterial Proteins, Cell Respiration, Gene Expression Regulation, Bacterial, Humans, Infant, Meningococcal Infections, Neisseria meningitidis, Nitric Oxide, Nitrite Reductases, Nitrites, Nitrous Oxide, Oxidation-Reduction, Oxidoreductases, Oxygen, Journal Article, Research Support, Non-U.S. Gov't

Identifiers

Local EPrints ID: 416384
URI: http://eprints.soton.ac.uk/id/eprint/416384
ISSN: 0950-382X
PURE UUID: fcb3ed1b-530a-4bbf-a83a-ee1b2894407a
ORCID for Robert C. Read: ORCID iD orcid.org/0000-0002-4297-6728

Catalogue record

Date deposited: 14 Dec 2017 17:30
Last modified: 10 Nov 2021 03:30

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Contributors

Author: Jonathan D. Rock
Author: M. Reda Mahnane
Author: Muna F. Anjum
Author: Jonathan G. Shaw
Author: Robert C. Read ORCID iD
Author: James W.B. Moir

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