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
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.
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Moir, James W.B.
f6831b5f-5cfd-4c56-b3cd-6782f413a07f
November 2005
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), .
(doi:10.1111/j.1365-2958.2005.04866.x).
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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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
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Local EPrints ID: 416384
URI: http://eprints.soton.ac.uk/id/eprint/416384
ISSN: 0950-382X
PURE UUID: fcb3ed1b-530a-4bbf-a83a-ee1b2894407a
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Date deposited: 14 Dec 2017 17:30
Last modified: 16 Mar 2024 04:10
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Contributors
Author:
Jonathan D. Rock
Author:
M. Reda Mahnane
Author:
Muna F. Anjum
Author:
Jonathan G. Shaw
Author:
James W.B. Moir
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